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Understanding Flowers and Flowering
Understanding Flowers
and Flowering
An Integrated Approach

Second Edition

Beverley Glover

1
Understanding Flowers and Flowering. Second Edition. Beverley Glover.
© Beverley Glover 2014. Published 2014 by Oxford University Press.
1
Great Clarendon Street, Oxford, OX2 6DP,
United Kingdom
Oxford University Press is a department of the University of Oxford.
It furthers the University’s objective of excellence in research, scholarship,
and education by publishing worldwide. Oxford is a registered trade mark of
Oxford University Press in the UK and in certain other countries
© Beverley Glover 2014
The moral rights of the author have been asserted
First Edition published in 2007
Second Edition published in 2014
Impression: 1
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a retrieval system, or transmitted, in any form or by any means, without the
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and you must impose this same condition on any acquirer
Published in the United States of America by Oxford University Press
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for information only. Oxford disclaims any responsibility for the materials
contained in any third party website referenced in this work.
 Preface

Flowers are the features of plants that most endear understanding why and how certain genetic com-
them to human beings. We grow flowers in our gar- ponents of the floral transition mechanism are con-
dens, we display them in our homes, and they fea- served and others are less so.
ture prominently in our artistic history. Scientists, I hope that this book might serve as a starting
too, have been fascinated by flowers, and there is a point for those interested in taking such an integrat-
long tradition of botanical study of floral structure ed approach to the study of flowers. I have writ-
and floral ecology. However, it is only in the last few ten it, and revised it for this second edition, with
decades that the tools of molecular genetics have the intention of helping to bridge the gaps between
been applied to flower induction, development, the different disciplines that work with flowers. My
and morphology. The data arising from these stud- aim is to provide students and researchers study-
ies, when combined with painstaking observation ing one aspect of floral biology with an overview
and analysis of the interactions of plants with their of other important aspects of flowers, both to help
pollinators, are beginning to provide the first truly them to set their own work in context and to en-
integrated understanding of both how and why courage them to consider experiments which might
flowers take the forms we so admire. lead to greater integration of the field. In particu-
Traditionally, flowers are studied from one of a lar, I hope that this book will encourage dialogue
number of viewpoints. Molecular biologists may between floral biologists of all varieties, with a
study the genetic control of flower induction or long-term view to ensuring a continuing increase in
flower development, usually focusing on a single interdisciplinary studies of flowers.
model species. Evolutionary biologists may study The book is divided into three main sections. Sec-
how flowers evolved, the forms of the earliest flow- tion I is introductory, giving some necessary back-
ers, or the morphology of flowers of ancient line- ground to the evolution of flowers and to the history
ages alive today. Pollination biologists may study of scientific thought on flowers and flowering. In
the interactions between plants and their pollinat- this second edition the chapter on the evolution of
ing animals, the natural selection exerted by those flowers has been extensively revised and updated.
pollinators, and how these pressures affect plant Section II considers the molecular mechanisms that
population dynamics. However, it is becoming control flower induction, flower development, and
clear that these various disciplines each have enor- floral mating type, providing coverage of the genet-
mous power to inform and shape the work of the ic material available for shaping by natural selec-
others. An understanding of how flower colour is tion. This section is initially focused on a very few
controlled biochemically and genetically, for ex- species of model plants, looking at the molecular
ample, can be of great benefit when studying how similarities which unite all flowers. In the later chap-
pollinator-imposed selection might have influ- ters it considers the development and reproductive
enced the evolution of petal colour within a group strategies of plants from a range of species, with a
of plants. Similarly, an understanding of how time new chapter on the floral transition in diverse spe-
of flowering influences competition with other spe- cies, and extensive revision of the chapter on floral
cies in the same community can be of great help in development in various groups. Section III extends

v
vi   P R E FA C E

this analysis much further, considering the expla- Waser, Enrico Coen, and the Cambridge University
nations for the differences between flowers, rather Botanic Garden for their great generosity in sharing
than their similarities. This section moves between images, Matthew Dorling and Heather Whitney for
molecular explanations for flower morphology and photographic assistance, Mike Webb for biochemi-
the ecological consequences of that morphology, cal pathways, and Rosie Bridge for line drawings.
in an attempt to integrate what we know both of For this second edition I owe a great debt to Alison
how and why different flowers take their different Reed, whose brilliant drawings and photographs
forms. A new chapter on the lability of floral form have greatly enhanced the figures throughout the
considers how floral traits change within phylo- book. Thanks also to Roy Barlow and Don Man-
genetic contexts. Finally, the epilogue attempts to ning for their excellent cover design for the first
draw out some themes which persist throughout edition, which has been adapted by the OUP team
the book, suggesting possible future directions for for edition 2. At Oxford University Press, Ian Sher-
the field. man has provided steadfast support for this project,
Many people have contributed to the develop- dealing with various changes to the schedule with
ment of both the first and second editions of this calm good humour, while Helen Eaton, Christine
book, and I am particularly grateful to all members Rode and Lucy Nash have kindly shepherded me
of my own research laboratory, past and present, through the production process. On a personal note
for enthusiastic support and helpful discussions I am still grateful to Jocelyn, Duncan, and Katie
at many points in the process. The second edition Taylor for lending me the space and quiet to re-
has benefited from the suggestions and advice of ally begin writing the first edition, rather than just
reviewers of the first edition, and I am particularly thinking about it. In recent years, and particularly
grateful to Doug Soltis, Elena Kramer, and Martin during the development of this second edition, I
Ingrouille for constructive comments. John Parker, have relied heavily on Sam Brockington and Ed-
Caroline Dean, David Hanke, Cathie Martin, Jeff wige Moyroud for the discussion of ideas and the
Ollerton, Rob Raguso, and Nick Waser read vari- development of new lines of thought, as well as
ous sections of the book in detail, and I must thank for practical and personal support in day-to-day
them all for the time and care that they took and for academic life. Thank you both. And finally, as with
their excellent suggestions and advice. Many peo- everything I do, the writing of a second edition has
ple were kind enough to provide me with images only been possible because of the patience and sup-
for figures. While these are acknowledged in the port of Stuart, Sam, and Katie—I do appreciate you
relevant figure legends, I particularly thank Nick all, really.
Contents

Preface v

SECTION I INTRODUCTION 1

1 The evolution of flowers 3

1.1 The origin of flowering plants 3

1.2 Seed plant reproductive structures 7
1.3 The first flowers 8
1.4 Floral diversification 12
1.5 Morphological diversity of the flower 13
1.6 An introduction to angiosperm phylogeny 13

2 Historical interpretations of flower induction and flower development 16

2.1 The foliar theory of the flower 16

2.2 The foliar theory in an evolutionary context 21
2.3 The transition to flowering 22
2.4 Developmental explanations of floral induction 22
2.5 Environmental explanations of floral induction 23
2.6 The florigen problem 25

SECTION II THE MOLECULAR MECHANISMS OF FLOWERING:

INDUCTION AND DEVELOPMENT 27

PART A Induction of Flowering 29

3 Flower induction in Arabidopsis thaliana 31

3.1 Arabidopsis thaliana as a model system for the study of flowering 31

3.2 Mechanisms of gene silencing 35
3.3 Flowering-time mutants 38

4 The autonomous pathways for floral inhibition and induction 43

4.1 The floral inhibition pathway 43
4.2 The autonomous induction pathway 47
4.3 Other endogenous factors that influence flowering time 50

vii
viii   C O N T E N T S

5 The photoperiodic pathway of floral induction 52

5.1 Sensing daylight 52

5.2 Measuring time 58
5.3 Integrating light and clock signals 60

6 The vernalization pathway of floral induction and the role of gibberellin 63

6.1 The vernalization promotion pathway 63

6.2 The gibberellin promotion pathway 67
6.3 Does gibberellin act in the vernalization promotion pathway
as well as independently? 69

7 Integrating the Arabidopsis thaliana flower induction pathways 70

7.1 Integrating the flowering-time pathways 70

7.2 Function of flowering-time integrators 71

8 Flower induction beyond Arabidopsis thaliana 77

8.1 The Arabidopsis flower induction model in other species 77

8.2 Flower induction in rice: a model short day plant 77
8.3 Flower induction in wheat and barley: a novel vernalization pathway 81
8.4 Flower induction in perennials 82
8.5 Flower induction in legumes 85
8.6 Flower induction in other species 85

PART B Development of Flowers 87

9 Changes at the shoot apical meristem in response to floral induction 89

9.1 Physiological changes at the shoot apical meristem 89

9.2 Shoot apical meristem anatomy 90
9.3 Gene expression patterns in the shoot apical meristem 91
9.4 Floral meristem identity genes act downstream
of the flowering-time integrators 92
9.5 Floral meristem identity genes 92

10 Development of the floral organs 102

10.1 The original ABC model of flower development 102

10.2 The role of D function genes 109
10.3 The role of E function genes 110
10.4 The role of cadastral genes 111
10.5 The quartet model of organ identity 113

11 The ABC model and the diversity of plant reproductive structures 115

11.1 Evolutionary history of MADS box transcription factors 115

11.2 ABC genes in gymnosperms 117
11.3 ABC genes in early diverging angiosperms 119
11.4 ABC genes in monocots 120
11.5 ABC genes in the basal eudicots 124
 C O N T E N T S    ix

11.6 Variations on the ABC model 124

11.7 Is A function unique to the Brassicaceae? 125

12 Function and development of gametophytes 127

12.1 Alternation of generations in multicellular organisms 127

12.2 Diversity of gametophyte form 129
12.3 The angiosperm female gametophyte 129
12.4 The angiosperm male gametophyte 132
12.5 Events following pollination 135

13 Outcrossing and self-fertilization 136

13.1 Reducing self-pollination in a hermaphroditic flower 136

13.2 Monoecy 138
13.3 Dioecy 140
13.4 Self-incompatibility (SI) 142
13.5 Sporophytic self-incompatibility (SSI) 142
13.6 Gametophytic self-incompatibility (GSI) 146
13.7 Heteromorphic self-incompatibility 148
13.8 Ensuring self-pollination 149

SECTION III POLLINATION SUCCESS: MOLECULAR AND ECOLOGICAL

INTERACTIONS 151

PART A How and Why Does Floral Form Vary? 153

14 Why are flowers different? Pollination syndromes: the theory 155

14.1 Cross-pollination 155

14.2 Abiotic pollen vectors 155
14.3 Biotic pollen vectors 157
14.4 Principles underlying the pollination syndrome concept 157
14.5 The pollination syndromes 158

15 Diverse floral shape and structure 167

15.1 Controlling corolla size 167

15.2 Controlling corolla symmetry 169
15.3 Controlling petal shape 172
15.4 Generating a nectar spur 173
15.5 Generating a composite inflorescence 174

16 Colouring the flower 176

16.1 Colour as a signal 176

16.2 Plant pigments 178
16.3 Carotenoid synthesis 178
16.4 Flavonoid synthesis 181
16.5 Betalains 185
x   C O N T E N T S

17 Enhancing flower colour 188

17.1 Mixing pigments 188

17.2 Co-pigmentation 189
17.3 Regulation of pigment distribution 189
17.4 The effects of metal ions 193
17.5 The importance of pH 194
17.6 The role of petal cell shape 196
17.7 Structural colour and structural enhancement of colour 198

18 Lability of floral form 200

18.1 Lability of floral size 200

18.2 Lability of floral symmetry 201
18.3 Lability of nectar spur length 204
18.4 Lability of flower colour 205
18.5 Lability of epidermal morphology 207
18.6 Lability of floral scent 209

PART B The Influence of Pollinators on Floral Form 211

19 Are flowers under selective pressure to increase pollinator attention? 213

19.1 Competition for pollinator attention 213

19.2 Facilitation of pollination 214
19.3 Techniques for investigating the role of pollinator attention
in limiting fitness 214
19.4 Evidence based on fruit and seed set following hand pollination 217
19.5 Evidence from mixed species plots 218
19.6 Analysis of character traits potentially displaced
by pollination competition 220

20 Do pollinators discriminate between different floral forms? 223

20.1 What pollinators see 223

20.2 What pollinators sense in other ways 225
20.3 Discrimination between petals of different colours 227
20.4 Discrimination between corollas of different sizes 232
20.5 Discrimination between zygomorphic and actinomorphic flowers 234
20.6 Discrimination between flowers with different petal cell shapes 234
20.7 Discrimination between flowers on the basis of scent 235

21 Pollination syndromes: the evidence 236

21.1 Historical context 236

21.2 Putting the assumptions together 237
21.3 Evidence for pollination syndromes 240
21.4 Evidence against pollination syndromes 241
21.5 The most effective pollinator? 243

Epilogue 245
References 247
Index 283
 (a) (b) (c)

Plate 1 The Gnetophytes. (a) Ephedra distachya subsp. monostachya (male). Photo by Le.Loup.Gris (Wikimedia Commons). (b) Welwitschia
mirabilis (male). Photo by Franzfoto (Wikimedia Commons). (c) Gnetum latifolium var. funiculare. Photo by Vinayaraj (Wikimedia Commons).
See also Figure 1.2.

Plate 2 The flower of Amborella trichopoda. Photograph kindly

supplied by Sangtae Kim and Pam Soltis (University of Florida).
See also Figure 1.4.

(a) (b) (c)

(d) (e) (f)

Plate 3 Species in which the floral transition has been studied. (a) Pisum sativum (Fabales). Photo by Rasbak. (b) Triticum species (Poales). Photo
by Optograph. (c) Populus species (Malpighiales). Photo by Matt Lavin. (d) Arabis alpina (Brassicales). Photo by Franz Xaver. (e) Oryza sativa (Poales).
Photo by C.T. Johansson. (f) Beta vulgaris (Caryophyllales). Photo by Forest and Kim Starr. All images from Wikimedia Commons. See also Figure 8.1.
 (a)

(b)

Plate 6 The long tasselled flowers of a wind-pollinated grass hang

far from the main body of the plant. See also Figure 14.1.

Plate 4 Early floral meristem identity mutants. (a) The Antirrhinum flo (a) (b)
mutant (left) has inflorescence shoots produced in place of the flowers
found in the axils of wild type bracts (right). Image kindly supplied by
Enrico Coen (John Innes Centre). (b) The Arabidopsis ap1 mutant is
slightly better converted to the floral form, with indeterminate floral
structures arising from the meristem. See also Figure 9.2.

(a) (b)

(c)

(c) (d)

(d) (e)

(e) (f)

Plate 5 The original ABC mutants. (a) apetala 1 (A function in Plate 7 Insect-pollinated flowers. (a) Magnolia (Magnoliales)
Arabidopsis). (b) ovulata (A function in Antirrhinum) (right) compared flowers are beetle-pollinated. (b) The fly-pollinated flowers of Fatsia
with wild type (left). (c) apetala 3 (B function in Arabidopsis). japonica (Apiales). (c) Bumblebee entering a Hebe flower (Lamiales).
(d) deficiens (B function in Antirrhinum) (right) compared with wild type (d) Many daisies (Asterales) are butterfly-pollinated. (e) The flowers of
(left). (e) agamous (C function in Arabidopsis). (f) plena (C function in Angraecum sesquipedale (Asparagales) have very long nectar spurs
Antirrhinum) (right) compared with wild type (left). Antirrhinum images and are pollinated by extremely long-tongued moths. Photographs (a),
kindly supplied by Enrico Coen (John Innes Centre). Image (e) provided (d), and (e) kindly supplied by Cambridge University Botanic Garden
by Ian Furner (University of Cambridge). See also Figure 10.2. and H. Rice. See also Figure 14.3.
 (b)
Plate 8 Vertebrate-pollinated flowers.
(a) The pendant form of Fuchsia
(a) flowers (Myrtales) is ideal for hovering
hummingbirds. (b) Bird of paradise (Strelitzia
regina, Zingiberales) flowers provide a sturdy
landing platform for non-hovering birds.
Photograph kindly supplied by Cambridge
University Botanic Garden. (c) The flowers
of Strongylodon macrobotrys, the jade
vine (Fabales), hang far below the foliage,
making them readily accessible to bats.
(c) See also Figure 14.4.

(a) (b)

Plate 9 Floral mimicry. (a) The titan arum

(Amorphophallus titanium, Alismatales)
attracts pollinators by releasing a strong
scent reminiscent of rotting flesh. Image
kindly provided by Cambridge University
Botanic Garden. (b) Ophrys episcopalis
(Asparagales), which mimics female
insects to achieve pollination through
pseudocopulation. Image kindly provided
by Richard Bateman (Royal Botanic Garden,
Kew). (c) The composite inflorescence of
Gorteria diffusa (Asterales) mimics its
(c) pollinating flies. See also Figure 14.5.
 (a)

(b)

Plate 12 The petals of Aquilegia formosa (Ranunculales) are heavily

modified to produce nectar spurs. Image kindly provided by Scott
Hodges (UCSB). See also Figure 15.4.
Plate 10 Zygomorphy and actinomorphy. (a) Many flowers are
radially symmetrical, or actinomorphic. (b) The flowers of Antirrhinum
species are bilaterally symmetrical, or zygomorphic. See also
Figure 15.2. (a)

(b)

Plate 13 Composite inflorescences in the daisy family. (a) The

Plate 11 The enantiostylous flower of Solanum heterodoxum capitulum of Gerbera hybrida, with zygomorphic outer florets
(Solanales). The style is the filamentous pink organ. Image kindly (each with one large petal) and actinomorphic inner florets. (b) The
provided by Sandy Knapp (Natural History Museum, London). capitulum of Senecio vulgaris usually contains only actinomorphic disc
See also Figure 15.3. florets. See also Figure 15.5.
(a) (b) (c)

Plate 14 Carotenoids give the yellow and orange colours to (a) Freesia (Asparagales), (b) Gerbera hybrida (Asterales), and (c) lilies (Liliales).
The photo in (b) is a modified version of a photo by Mauro Girotto (Wikimedia Commons). See also Figure 16.2.

(a) (b)

(c)

Plate 15 Anthocyanins give the purple, magenta, and pink colours to (a) Petunia hybrida (Solanales, delphinidin and petunidin), (b) Antirrhinum
majus (Lamiales, cyanidin), and (c) Pelargonium (Geraniales, pelargonidin). The photo in (c) is adapted from a photo by Rameshng (Wikimedia
Commons). See also Figure 16.4.
 (a) (b) (c)

Plate 16 Betalains give the yellow, purple, and pink colours to (a) Portulaca oleracea, (b) Mirabilis jalapa, and (c) Sesuvium portulacastrum
(all Caryophyllales). All images kindly provided by Sam Brockington (Cambridge). See also Figure 16.6.

(a) (b)

(c) (d)

Plate 17 Pigment regulation. (a) Viola cornuta ‘Yesterday, Today and Tomorrow’ is fully purple 5–8 days after pollination (left), but opens
as a white flower (middle) in which pigmentation steadily increases (right). Image kindly provided by Martha Weiss (Georgetown University,
Washington, DC). (b) The delila mutant of Antirrhinum lacks pigmentation in the tube as a result of loss of activity of a bHLH transcription factor.
(c) The Venosa locus produces pigmentation over the petal veins in a pale Antirrhinum flower. VENOSA encodes a MYB transcription factor.
(d) The an11 mutant of petunia lacks pigmentation as a result of loss of activity of a WD40 protein. The transposon in the AN11 locus excises
somatically, generating patches of wild type red tissue. Image kindly provided by Ronald Koes (Vrije Universiteit, Amsterdam). See also Figure 17.1.
 (a) (b)

(c) (d)

Plate 18 Metals and pH both affect flower colour. (a) The Himalayan blue poppy owes its blue colour to an interaction between anthocyanin and
iron. Photograph kindly supplied by Cambridge University Botanic Garden. (b) Hydrangea flowers can be blue or pink, depending on the metal ions
present in the soil. (c) Morning glory flowers have a high vacuolar pH. Image kindly provided by Felix Jaffe. (d) An unstable pH4 mutant of petunia,
with revertant wild type red (acidic) sectors on a mutant bluish-pink (more alkaline) background. Image kindly provided by Ronald Koes (Vrije
Universiteit, Amsterdam). See also Figure 17.2.
 (a) (b)

(c)

Plate 19 Petal cell shape affects flower

colour. (a) Wild type Antirrhinum petal
epidermis, composed of conical cells. (b) mixta
mutant petal epidermis, composed of flat
cells. (c) Wild type (left) and mixta mutant
(right) flowers, showing the difference in
colour attributable to the cell shape. See also
Figure 17.3.

(a) (b)

(c) (d)
Sunlight
Chin

+/– 15º

Ranunculus
ower

Plate 20 Structural colour. (a) Tulip ‘Queen of the Night’ has iridescent rainbow colours on top of purple pigmentation. (b) This iridescent effect
is caused by a diffraction grating. (c) The bright yellow buttercup reflects yellow light very strongly. (d) The buttercup acts as a double mirror,
reflecting yellow and white light together on to nearby surfaces such as a child’s chin. See also Figure 17.4.
(a)

(b)

(c)

(d)

Plate 21 Variation in zygomorphy in the Antirrhineae. (a) Highly

zygomorphic Antirrhinum majus. (b) Moderately zygomorphic Maurandya
scandens. (c) Slightly zygomorphic Mabrya acerifolia. (d) Almost
actinomorphic Rhodochiton atrosanguineum. All scale bars 1 cm.
See also Figure 18.1.

(a) (b)

Plate 22 Variation in nectar spur length.

(a) Gymnadenia conopsea flowers have very
long nectar spurs. (b) Gymnadenia rhellicani
flowers have almost no nectar spur. Images
kindly provided by Matt Box (Sainsbury
Laboratory, Cambridge University). See also
Figure 18.3.
 DHQ

F3¢5¢H

DHM
DHK
DFRI
F3¢H
MALVIDIN
DHQ

DHK

F3¢H
CYANIDIN
DHQ
DFR2 Plate 23 Development of the Clarkia gracilis
petal spot. Early expression of DFR2 in the spot
CYANIDIN region, in the presence of F3′H but not F3′5′H,
results in red cyanidin pigment. Later expression
of DFR1 throughout the petal, in the presence
of F3′5′H, results in mauve malvidin production.
EARLY LATE See also Figure 18.4.

(a) (b)

(c) (d)

Plate 24 Flowers for which pollinators have been shown to discriminate between colour morphs. (a) Mimulus lewisii. (b) Mimulus cardinalis.
Images (a) and (b) kindly provided by Toby Bradshaw (Washington State University). (c) Antirrhinum majus wild type and incolorata lines.
(d) Antirrhinum majus wild type and sulfurea lines. Images (c) and (d) kindly provided by Enrico Coen (John Innes Centre). See also Figure 20.2.
 (a) (b)

Plate 25 Flowers with significant nectar guides. (a) Delphinium nelsonii. Image kindly supplied by Nick Waser (University of California – Riverside).
(b) Clarkia xantiana subsp. xantiana. Image kindly provided by Vince Eckhart (Grinnell College, USA). See also Figure 20.3.

Plate 26 Flowers for which pollinators have been shown to discriminate

on the basis of size. Ipomopsis aggregata. Image kindly provided by Nick
Waser (University of California – Riverside). See also Figure 20.4.
 (a) (b)

Plate 27 Plants for which the main pollinator type can be accurately predicted from floral morphology. (a) Penstemon centranthifolius
(hummingbird-pollinated). (b) Penstemon heterophyllus (bee-pollinated). Images (a) and (b) kindly supplied by Scott Armbruster (University of
Portsmouth). See also Figure 21.1.

(a) (b)

Plate 28 Plants that have cast doubt on the pollination syndrome concept.
(a) Viola cazorlensis. Image kindly supplied by Carlos Herrera (Seville). (b) Microloma
sagittatum with its sunbird pollinator. Image kindly supplied by Anton Pauw
(Stellenbosch). See also Figure 21.2.
SECTION I

Introduction
 C H A PT ER 1

The evolution of flowers

The oldest fossil flower currently known is around of these traits are shown in Fig. 1.1. They have fully
125 million years old. Flowers, and the plants that protected and enclosed ovules with two layers of
produce them (angiosperms or flowering plants), protective integuments surrounding them, enclosed
are relatively recent innovations in evolutionary in a carpel within which the seed eventually devel-
terms. The first land plants, which did not possess ops. Their wood contains true, continuous vessels,
flowers, arose around 470 million years ago, but as well as the more widespread tracheids in which
fossil evidence indicates that only after another 340 water has to cross a membrane between individual
million years did the angiosperms appear. However, cells. Their phloem consists of sieve tube elements
following their appearance in the fossil record of the and the unique companion cells, both derived from
early Cretaceous period, the angiosperms spread the same mother cell. Angiosperms have distinctive
geographically from their point of origin in the pollen, with columnar structures providing sup-
tropics and diversified dramatically to become the port for the surface layer. In addition, only angio-
ecologically dominant plant group in the great ma- sperms undergo double fertilization, whereby two
jority of terrestrial habitats. This extraordinary geo- genetically identical sperm cells are released into
graphic and morphological radiation took a mere 40 the ovary with one fertilizing the egg and the other
million years, and was even more extraordinary for fusing with the central cell to form the endosperm.
the number of species it generated. The 250–400,000 Traditionally, fossil evidence was all that was avail-
species of extant angiosperms represent the most able to probe the origins of the angiosperms, but,
species-rich plant group by far, and are exceeded in more recently, molecular data obtained from extant
numbers in the speciose animal kingdom only by the species have been used to inform the debate. The
arthropods. Furthermore, the differences in growth following two sections consider insights from these
habit, morphology, and life history within the an- two types of evidence into the age and nature of the
giosperms are vast, leading Darwin to describe the earliest angiosperms, and their relationships with
speed and scale of this recent radiation as ‘an abomi- other seed plants.
nable mystery’. It is not possible to provide here a
full analysis of the extensive literature on the origins
1.1.1 Fossil evidence for angiosperm origins
and radiation of angiosperms and their flowers. The
aim of this chapter is to provide an overview of the Fossil evidence dates the origin of the angiosperms
key issues surrounding the origin of the flowering to the early Cretaceous period, with the oldest fossil
plants and their flowers, and to conclude with an in- flowers (125 million years ago), angiosperm fruits
troduction to the major groups of flowering plants, (121 million years ago), angiosperm pollen (130 mil-
many of which will be referred to in later chapters. lion years ago), and angiosperm leaves (120 million
years ago) all supporting this conclusion (Hughes
1994; Krassilov and Dobruskina 1995; Brenner 1996;
1.1 The origin of flowering plants
Friis et al. 1999, 2001; Sun et al. 2002). The oldest fos-
Angiosperms are defined by a number of features, sils suggest that the first angiosperms were aquatic
of which possession of a flower is only one. Some plants. For example, Archaefructus, a fossil dated to

Understanding Flowers and Flowering. Second Edition. Beverley Glover.

© Beverley Glover 2014. Published 2014 by Oxford University Press.
4   I N T R O D U C T I O N

(a) (b)
Pollen grain
Stigma

Style Sperm
Pollen tube Sperm nuclei
Egg

Ovules

Antipodals
Ovary

Embryo sac

(c) (d)

Tectum

Columella

Foot layer
Intine

Figure 1.1 Some defining features of angiosperms. (a) Enclosed ovules, enfolded within the carpel. (b) Double fertilization, with two sperm nuclei
arriving in the pollen tube. One fertilizes the egg cell and the other fertilizes the central cell with its two nuclei, generating the triploid endosperm.
(c) Columnar pollen exine, shown in cross section. (d) Wood with true vessels as well as the narrower tracheids found in gymnosperms.

124.6 million years ago, has the long thin stems and the angiosperms). If the eudicots were already pre-
highly dissected compound leaves that are typical sent in the early Cretaceous period, it is likely that
of aquatic species. Perhaps even more convincingly, the first angiosperms arose considerably earlier.
it is found with fossilized fish mixed in with the Molecular analyses also date the origin of the an-
plant tissue (Sun et al. 2002). Similarly, Friis et al. giosperms a little earlier than 130 million years ago
(2001) identified a fossil flower from deposits up (see Section 1.1.2 below).
to 125 million years old as a member of the Nym- The fossil record suggests that the angiosperms
phaeales (the modern water lilies), on the basis of rapidly diversified from their aquatic origins to oc-
its unique centrally protruding floral axis and its cupy understorey and early successional niches on
distinctive seeds with wavy cell walls in their seed dry land, with this first diversification occurring
coats. during the early Cretaceous period (Friis et al. 2005).
The recent identification of Leefructus mirus, a Their subsequent radiation over the course of the
fossil with features diagnostic of the eudicot order Cretaceous quickly led to the adoption of late suc-
Ranunculales, in deposits dated at 122–125 million cessional ecological positions, presumably as their
years old, suggests that the angiosperms might be size and woodiness increased. The scarcity of angio-
older than paleontologists had previously thought sperm wood in the early Cretaceous fossil record,
(Sun et al. 2011). The eudicots are a more recently along with the apparently small size of early an-
derived group of the angiosperms (see Section 1.6 giosperm seed and leaves, supports the conclusion
and Fig. 1.5 for an overview of relationships within that the early angiosperms were small herbaceous
 T he evolution of flowers    5

s­ pecies with a weedy lifestyle, whether on land or in of the angiosperms, on the basis of both fossil and
fresh water. Some authors have speculated that this morphological evidence (Crane et al. 1995). There
herbaceous habit followed an early loss of woodi- are currently three extant genera of gnetophytes,
ness, since most gymnosperms are woody and most namely Gnetum, Ephedra, and Welwitschia, which
of the earliest diverging groups of extant angio- share a range of morphological similarities with
sperms are also woody (Willis and McElwain 2002). some angiosperms (see Fig. 1.2). In particular, leaf
The first angiosperms appear to have originated morphology and venation in Gnetum closely resem-
in tropical regions, only spreading to higher lati- ble that of angiosperms, their xylem does contain
tudes after 20–30 million years (Barrett and Willis vessels, and some gnetophytes produce reproduc-
2001). The earliest angiosperm fossils (of pollen) tive structures containing both male and female
have been found in modern-day Israel and Mo- parts. Double fertilization, often considered to be
rocco, land that lay just north of the equator in the a defining feature of angiosperms, has also been
early Cretaceous period. The subsequent spread documented in both Ephedra and Gnetum (Fried-
of the angiosperms into higher latitudes was very man 1990). However, recent molecular studies have
rapid, accompanied by an increasing dominance of refuted this hypothesis (see below), and have even
those areas already occupied (as measured by the questioned the status of the Gnetophytes as a di-
relative proportions of angiosperm and other pol- vision, suggesting that they are part of the Conif-
len types retained in the fossil record) (Willis and erophytes (Qiu et al. 1999; Chaw et al. 2000). These
McElwain 2002). recent studies confirm the monophyletic nature of
The identity and morphology of the last com- the extant gymnosperms, indicating that none of
mon ancestor of the angiosperms and other land them provide a clear link to the angiosperms.
plant groups have long been a source of debate. The fossil record informs the debate on the re-
The most closely related extant group is the gym- lationship of angiosperms to other land plant lin-
nosperms, traditionally viewed as a cluster of three eages by providing details of extinct groups. Two
or four divisions. Of these divisions, the conifers extinct gymnosperm groups in particular, the Ben-
(Coniferophytes) are familiar, and dominate many nettitales and the Mesozoic ‘seed ferns’ (such as
high-latitude forests. The cycads (Cycadophytes) Caytonia), have frequently been proposed as ances-
are currently less prominent, but fossil records tors or close relatives of the angiosperms, and sev-
indicate that they were once ecologically highly eral studies based on fossil and extant morphology
significant. The Ginkgophytes are currently repre- linked the Bennettitales, the Gnetophytes, and the
sented by only one surviving species, Ginkgo biloba, angiosperms into a clade known as the anthophytes
a commonly grown tree in parks and gardens. The (Crane 1985; Doyle and Donoghue 1986). These
remaining group, the Gnetophytes, was, until re- conclusions were based on the distinctive morphol-
cently, considered likely to be the closest relative ogies of the extinct plants, analysed by painstaking

(a) (b) (c)

Figure 1.2 The Gnetophytes. (a) Ephedra distachya subsp. monostachya (male). Photo by Le.Loup.Gris (Wikimedia Commons). (b) Welwitschia
mirabilis (male). Photo by Franzfoto (Wikimedia Commons). (c) Gnetum latifolium var. funiculare. Photo by Vinayaraj (Wikimedia Commons).
See also Plate 1.
6   I N T R O D U C T I O N

microscopical observation of fossils. Caytonia, for different evolutionary rates, and concluded that the
instance, has ovules almost entirely enclosed with- angiosperms originated 167–199 million years ago
in cupules, bearing some similarity to angiosperm (Bell et al. 2010). The same study dated the origin of
carpels. The Bennettitales have many morphologi- key angiosperm clades, with the eudicots appear-
cal features in common with angiosperms, most ing around 130 million years ago, the Rosids arising
notably the production of a bisexual reproductive 108–121 million years ago, and the Asterids appear-
shoot surrounded by sterile (possibly perianth-like) ing 101–119 million years ago (see Section 1.6). These
organs. Because these fossil taxa cannot be incorpo- dates are highly compatible with the fossil record,
rated into molecular phylogenies, attempts to in- suggesting only that the very earliest angiosperms
tegrate them into our understanding of seed plant have not yet been retrieved from fossils. The dating
relationships requires a combined molecular/mor- of the eudicots at 130 million years old is particu-
phological approach. Such approaches often pro- larly interesting, given the recent discovery of the
duce conflicting results, but it is certainly likely that eudicot fossil Leefructus mirus from deposits 122–125
some of these extinct lineages represent branches of million years old (Sun et al. 2011).
the land plant phylogeny that diverged along the If the angisoperms originated 167–199 million
branch leading to angiosperms. years ago, the absence of angiosperm fossils from
deposits earlier than 130 million years can be read-
ily explained in a number of ways. It is possible that
1.1.2 Molecular evidence for angiosperm origins
the fossil record does not contain the very earliest
Molecular evidence for the origins of angiosperms angiosperms because they were not woody, were
is based on the comparison of DNA sequences or relatively rare within their communities, or were
fingerprints from extant species. In addition, use of predominantly found in dry or alpine environments
a molecular clock, which calculates the age of diver- not conducive to fossil formation. Some authors
gence of two sequences according to the number of have suggested that their early Cretaceous diversi-
differences between them, can provide estimates of fication actually represents a migration event from
the date of evolutionary events. Recent molecular a previous habitat less suited for fossil formation.
dating studies have used methods to allow for di- The molecular phylogenies of Qiu et al. (1999)
vergent evolutionary rates, particularly those aris- and Chaw et al. (2000) have also shed light on ques-
ing following branching of a lineage, when different tions of relatedness between gymnosperm groups
branches might experience very different evolution- and the early angiosperms (see Figs. 1.2 and 1.3).
ary rates according to whether they adopt a woody
(long generation time) or herbaceous (short genera-
ANGIOSPERMS
tion time) habit (Smith and Donoghue 2008).
Early molecular dating studies indicated an ori-
gin of the angiosperms considerably earlier than the GNETOPHYTES
130 million years ago that the fossil record suggests.
Studies indicated variously that the angiosperms
CONIFEROPHYTES
arose in the late Carboniferous period, 290 million
years ago (Kenrick 1999; Qiu et al. 1999), and that the
monocotyledonous angiosperms diverged from the GINKGOPHYTES

dicotyledonous species 250–200 million years (Wolfe

et al. 1989) or 300 million years ago (Martin et al. CYCADOPHYTES
1989). However, improvements in dating technology
are mainly responsible for the convergence of recent Figure 1.3 Molecular evidence and morphological evidence
suggest different relationships between the angiosperms and the
reports on an age for the angiosperms of 140–180
various groups of extant gymnosperms. Molecular data (left) place
million years (Sanderson et al. 2004; Bell et al. 2005a). the angiosperms as sister group to the monophyletic gymnosperms,
The most recent detailed study used a ‘relaxed clock’ whereas traditional morphological analysis (right) placed the
method that allowed different ­lineages to experience angiosperms and the gnetophytes as sister taxa.
 T he evolution of flowers    7

To the astonishment of many botanists, the extant they were probably woody, not herbaceous, despite
gnetophytes resolved in a single clade with the the relative scarcity of early fossilized angiosperm
conifers, refuting the suggestion that their ances- wood. Following the publication of the phylogeny
tors were the precursors of the angiosperms. In- of Qiu et al. (1999), the position of Amborella as the
stead, the extant gymnosperms have been shown most basal extant angiosperm was controversial for
to be monophyletic and to have diverged from the a while. Goremykin et al. (2003) analysed 61 protein-
total land plant lineage around 300 million years coding genes common to 13 fully sequenced land
ago. They can therefore be thought of as the sister plant chloroplast genomes, which placed the ori-
group to angiosperms, and do not necessarily pro- gin of Amborella later than the origin of the mono-
vide much relevant information about the likely cots. However, the controversy was short-lived
morphology of the ancestral angiosperm. Indeed, and the position of Amborella as sister to the other
the derived nature of many extant gymnosperm angiosperms has been confirmed by numerous
reproductive structures, combined with the par- other studies (see detailed discussion in Stefanovic
tial nature of the fossils of extinct gymnosperms, et al. 2004; Soltis and Soltis 2004; Soltis et al. 2004;
makes it very hard to draw conclusions even about Martin et al. 2005; Lockhart and Penny 2005). This
the nature of ancestral gymnosperm reproductive controversy highlights some of the important con-
structures. siderations involved in designing approaches to re-
The phylogeny of Qiu et al. (1999) provides use- construct phylogeny, and also emphasizes the point
ful information on the relationships of early di- that any phylogenetic tree can only be viewed as
verging angiosperm clades, which can be used to the current best hypothesis based on available data.
infer features of ancestral angiosperm reproductive
structures. The Nymphaeales (water lilies) are in-
1.2 Seed plant reproductive structures
deed ancestral to many other plant groups, but are
not the sister group of all the other angiosperms. The reproductive structures of most plant lineages
This position was awarded to Amborella trichopoda, prior to the angiosperms, including most of the
the only extant species of the Amborellales, and a gymnosperms, were unisexual. The evolution of
native of New Caledonia (see Section 1.6; Fig. 1.4). seeds freed plants to reproduce in the absence of a
Amborella is a small weedy shrub, supporting the film of external water (previously necessary to al-
idea that the basal angiosperms were understorey low fragile free-swimming male gametes to fuse
or early successional species, but indicating that with a static egg). In seed plants the female gameto-
phyte is surrounded by parental sporophyte tissue,
usually derived from bracts. These enfolding bracts
act to protect the ovule and may also serve as a
protective coat when the seed is dispersed. In gym-
nosperms the ovule is not completely enclosed in
sporophyte tissue, but is protected within a cham-
ber, into which wind-blown pollen is drawn after
being trapped by a drop of secreted liquid.
In the cycads, dioecy is the rule, with female
plants producing clusters of ovules on the edges
of modified leaves called megasporophylls. The
whole female reproductive structure forms an ovu-
late cone. Male plants produce cones of differently
specialized leaves, the scale-like microsporophylls,
arranged in a spiral phyllotaxis to produce a cone.
Figure 1.4 The flower of Amborella trichopoda. Photograph kindly
These microsporophylls possess a pollen sac on
supplied by Sangtae Kim and Pam Soltis (University of Florida). their abaxial surface, each of which produces nu-
See also Plate 2. merous pollen grains. A similar system operates
8   I N T R O D U C T I O N

in Ginkgo, although the ovules are born in pairs unisexual reproductive cones occur either together
on stems rather than as a cone. In contrast, most on a single plant or each on a separate plant. The
conifers are monoecious, producing male and fe- combination of male and female organs on a single
male cones on the same individual plant, although shoot is an angiosperm innovation. The develop-
some taxa within the group are dioecious (such as ment of a single shoot containing both male and fe-
the junipers and yews). The Gnetophytes are usu- male reproductive organs was therefore a key event
ally dioecious, although some species of the genus in the evolution of flowers.
Ephedra are monoecious. Analysis of cone struc- Discussion of the development of a bisexual re-
ture has revealed that the pollen cone of conifers productive shoot is complicated by the lack of clear
is a condensed branch with the microsporophylls homology between gymnosperm cones and angio-
representing the modified leaves along the branch. sperm flowers. Since the cones of cycads and the
However, the seed cone of conifers, and both cone pollen cones of conifers are condensed branches
types in the Gnetophytes, are thought to be derived with the scales representing leaves, they could
from a condensed branch with branches. In this sce- be described as homologous to a flower (with the
nario the central stem produces bracts with modi- reproductive and perianth organs derived from
fied stems in their axils—the modified stems are the leaves). However, the compound cones of the Gne-
scales of the cone (Judd et al. 2007). tophytes and female conifers are clearly not ho-
mologous to flowers. In these cones the scales are
modified stems, and so the structure is much more
1.3 The first flowers
like an angiosperm inflorescence, where each flow-
Despite the absence of a clear picture of the last er is formed from a separate axillary meristem.
common ancestor of angiosperms and gymno- Whatever the homology relationships, the evolu-
sperms, there are clearly some key innovations that tion of the flower required the development of a bi-
arose in the angiosperm lineage and gave rise to sexual shoot, which may then have required much
flowers, such as the combining of male and female subsequent reduction to form the flowers we see
reproductive structures within a small space on the today. Assuming that the ancestor of angiosperms
same shoot and the production of perianth organs and gymnosperms produced its male and female
(Theissen et al. 2002). Indeed, it is these innovations reproductive structures on separate shoots, each
that give us the modern definition of a flower (the composed of a spiral of organs, then the develop-
bisexual reproductive shoot of an angiosperm, in which ment of a bisexual shoot (and later flower) requires
the reproductive organs are surrounded by whorls of ster- either the development of female organs at the top
ile organs). Analysis of the development of these in- of the male shoot or the development of male or-
novations allows us to build a general picture of the gans at the base of the female shoot. All angiosperm
evolution of the first flowers. flowers contain an outer whorl of male reproduc-
tive organs and an inner whorl of female repro-
ductive organs, suggesting that this evolution of
1.3.1 A bisexual reproductive shoot
bisexual flowers occurred only once (Cronk 2001).
The typical angiosperm flower is hermaphrodite, A single exception to this rule (with male reproduc-
and this is believed to be the ancestral condition tive structures inside a whorl of female ones) has
for flowers. Although there are many examples been identified in the inside-out flower of Lacan-
of derived unisexual flowers—either on hermaph- donia schismatica (Pandanales), as a result either of
roditic plants (monoecy) or on unisexual plants homeotic organ conversion or of reduction of the
­(dioecy)—the majority of angiosperm flowers pro- inflorescence to resemble a flower (for a review, see
duce both male and female reproductive organs. Garray-Arroyo et al. 2012).
This is in marked contrast to the reproductive An adaptive explanation for the combination of
structures of most other plant lineages, where uni- male and female reproductive organs in the same
sexual reproductive structures are the norm. In the shoot was proposed by Frohlich (2002), who ob-
gymnosperms, as described above, the two types of served that ectopic sterile ovules are sometimes
 T he evolution of flowers    9

produced by the male reproductive cones of the ­radiata, PrFLL is expressed in male cones only, and
gnetophyte Welwitschia, and appear to attract pol- a duplicate gene, NEEDLY, which has been lost
linating insects to the male branches by exuding the from the angiosperm lineage, is expressed only in
same droplets of liquid that are secreted by fertile female cones. Frohlich interpreted these observa-
female ovules (Endress 1996). This would provide tions as implying that the angiosperm flower is de-
a selective advantage in terms of male fitness (pol- scended from an ancestor of the male gymnosperm
len export) to a male shoot with additional female cone. In the ancestral angiosperm lineage the genes
characters. From there it is easy to imagine the full responsible for ovule development were recruited
feminization of the ectopic ovules into fertile struc- to the control of PrFLL, resulting in the production
tures. Bisporangiate cones are also occasionally of ectopic ovules, and eventually the evolution of
produced by other gymnosperms, and the pres- carpels. However, more recent data have largely
ence of ovule droplets is commonly reported in disproved the exclusively male expression of PrFLL
these cones (Rudall et al. 2011). Flores-Renteria et al. and the exclusively female expression of NEEDLY
(2011) even observed that the bisporangiate cones in gymnosperms. First, Shindo et al. (2001) showed
of Pinus johannis were fully fertile, unlike the sterile that the PrFLL-like gene of Gnetum parvifolium is
ovules in male cones reported in Welwitschia. Other expressed in the female reproductive structure,
authors have noted that bisexual shoots facilitate rather than the male one. Dornelas and Rodriguez
selfing, which is potentially of great importance to (2005) similarly showed that the PrFLL-like gene of
plants (like the early angiosperms) invading new Pinus caribaea is expressed in female, but not male,
habitats. cones. Vazquez-Lobo et al. (2007) reported expres-
Several models have been proposed to explain sion patterns for the PrFLL-like and NEEDLY genes
the evolution of the bisexual shoot from a molecu- from Picea abies, Podocarpus recihii and Taxus globosa,
lar genetic perspective. These focus on two sets of finding that both genes are expressed in both male
genes—those controlling the conversion of the mer- and female reproductive structures of all three spe-
istem to the reproductive form (particularly LEAFY; cies. A recent comparison of transcriptome profiles
see Chapters 7 and 9), and those controlling the pro- of the male and female cones of Ginkgo biloba, the
duction of male organs in the angiosperm flower cycad Zamia fisheri and the gnetophyte Welwitschia
(B function genes; see Chapter 10). This section will mirablis with the transcriptomes of flowers of Arabi-
outline these models, but the reader might find the dopsis thaliana (Brassicales) and Oryza sativa (Poa-
models clearer when they have read later chapters les) detected no significant differences between the
on floral meristem and floral organ development. proportion of gymnosperm orthologous genes that
The first model to take a genetic approach to the were expressed both in the male cone and in the
evolution of bisexual flowers was the Mostly Male angiosperm flowers, and the proportion of gymno-
Theory. In this model the bisexual shoot evolved sperm orthologous genes that were expressed both
by the production of ectopic ovules in the centre in the female cone and in the angiosperm flowers
of a male cone, the cone retaining a ‘mostly male’ (Tavares et al. 2010). From this analysis the authors
identity (Frohlich 2002). This hypothesis was based concluded that the angiosperm flower was not a
on analysis of sequence and expression patterns of ‘mostly male’ structure, as its transcript content did
genes predicted to regulate gymnosperm cone de- not more closely resemble a male cone than a fe-
velopment, which suggested that an angiosperm male cone.
gene required for flower production (LEAFY) is If the bisexual shoot did not evolve by the ec-
most closely related to a gymnosperm gene in- topic development of ovules on a male cone (or
volved in male (but not female) cone development vice versa), it must have evolved by the conver-
(Frohlich and Parker 2000). The PrFLL gene of Pinus sion of organs at the axis of a male cone into the
radiata (and the equivalent gene in Welwitschia and female form, or by the conversion of the organs at
Ginkgo) is very similar to the angiosperm LEAFY the base of a female cone into the male form. These
gene, which encodes a protein crucial in deter- homeotic models do not imply that the flower is
mining the floral nature of the meristem. In Pinus predominantly male or female, but that c­ onversion
10   I N T R O D U C T I O N

of one organ type into the other results in a more hypotheses. Loss of B function gene expression
nearly equal shoot. They are therefore more com- from the upper regions of a male axis would result
patible with the transcriptomic analysis of Tavares in the production of female organs within whorls
et al. (2010). Theissen et al. (2002) described these of male organs. Similarly, gain of B function gene
ideas as the ‘Out of Male’ hypothesis and the ‘Out expression in the lower regions of a female axis
of Female’ hypothesis, depending on the shoot type would result in the production of male organs out-
in which the conversion occurred. Homeotic con- side whorls of female organs (Theissen et al. 2002).
version of organ types is not usually attributed to The current lack of functional tools with which to
meristematic function genes like LEAFY, but to the explore gymnosperm cone development limits our
genes controlling floral organ development that are ability to test these various hypotheses.
discussed in Chapter 10. The key set of genes to this
discussion are called the B function genes, and in
1.3.2 Evolution of the perianth
the angiosperm flower they specify the develop-
ment of the stamens (male reproductive structures) The typical angiosperm flower produces two whorls
in conjunction with the expression of C function of sterile protective perianth organs—often, but
genes. They also specify petal development, but not always, differentiated into protective green se-
that is incidental to this discussion. The C function pals and attractive petals. The production of these
genes alone specify carpel development (female perianth organs was another angiosperm innova-
­reproductive structure ­development). Both B and C tion. However, it is not necessary to assume that
function genes encode transcription factors called the first angiosperm flower possessed a perianth.
MADS box proteins, which activate transcription Indeed, some authors have argued to the contrary,
of the downstream genes involved in organ iden- proposing a perianth-less structure containing both
tity (see Chapters 10 and 11 for further details). male and female reproductive organs as the first
Genes related to angiosperm B function genes have flower (Theissen et al. 2002). Some fossil evidence
been isolated from conifers, and from Gnetum, and does seem to support this hypothesis, including the
are expressed in the male cones, but not in the fe- morphology of Archaefructus and other early fossil
male cones (Sundstrom and Engstrom 2002; Winter angiosperms (Sun et al. 1998). Other authors have
et al. 2002). Similarly, genes related to angiosperm argued that the specialized habitats of early fossil
C function genes have been isolated from Gne- angiosperms, particularly the aquatic ones, might
tum, Cycas, and Picea, and shown to be expressed have resulted in specialized floral morphology and
in both the female cones and the male cones, indi- even secondary loss of a perianth. However, it is
cating that C function is active in all reproductive clear that at some point the bisexual reproductive
structures in gymnosperms (Rutledge et al. 1998; shoot was surrounded by sterile organs to generate
Tandre et al. 1998; Zhang et al. 2004). The true roles the familiar form of the angiosperm flower.
of these genes in gymnosperms remain hypotheti- The development of the perianth may have
cal, as no functional tests have yet been possible. occurred in a number of ways. One hypothesis pro-
However, on the basis of expression patterns alone, poses that the perianth developed by loss of repro-
it appears that expression of the C function genes, ductive function of the outermost male organs, a
in angiosperms and in gymnosperms, confers a re- model that has molecular support from studies of
productive identity on an organ. It is expression of ranunculid flower development (Kramer and Irish
the B function gene that determines which sort of 1999). Alternatively, bract-like structures may have
reproductive structure is produced. Expression of B been modified to produce a perianth, shifiting posi-
function genes as well as C function genes results in tion on the shoot to develop immediately outside
the development of a male reproductive structure, the reproductive organs. Both mechanisms have
a pollen cone. Expression of C function genes alone some support, and some authors postulate that the
results in the development of a female reproductive perianth evolved multiple times. However, a re-
structure, a seed cone. These observations provide view of the available evidence (Specht and Bartlett
the basis for the Out of Male and Out of Female 2009) suggests that the ancestral flower did have a
 T he evolution of flowers    11

­ erianth (that is, there was a single ancestral origin),

p It was noted in Section 1.1.1 that similar flower-
and that this perianth was lost repeatedly in multi- like structures also evolved in the now extinct
ple lineages, including some of the earliest diverging Bennettitales, a group of gymnosperms that were
groups (see Section 1.6), such as the Hydatellaceae widespread between 248 and 140 million years ago
(Nymphaeales) and the Chloranthaceae (Chloran- (Willis and McElwain 2002). Some species of this
thales). Given the great morphological similarities group combined both male and female reproduc-
between sepals and leaves, most authors now agree tive organs on a single axis, and appear to have
that the sepals (and thus the ancestral perianth) are enclosed those organs within a circle of bracts, su-
derived from bracts. During subsequent evolution perficially like angiosperm flowers. There is debate
of the angiosperm flower a differentiated perianth as to whether these bracts opened, like the perianth
arose in multiple lineages. The inner organs of this organs of flowers, or whether structural constraints
differentiated perianth, the petals, are thought to would have prevented this. It is also unclear wheth-
have evolved from both sepals and stamens in dif- er the bracts contained pigmentation, believed to
ferent lineages (see Section 1.3.3). be a significant factor in the success of angiosperm
flowers.

1.3.3 Early ‘flower’ morphology

1.3.4 Evolution of the differentiated perianth
The first angiosperm flowers with perianth organs
almost certainly did not have separate sepals and The perianth of most angiosperms is clearly divided
petals, but an undifferentiated and unspecialized into protective green sepals and attractive colour-
perianth. Analysis of the fossil record and of ex- ful petals. However, this differentiation of roles is
tant basal angiosperms suggests that the anthers of a derived feature that appears to have been gained
these flowers made a lot of pollen, while the ovules and/or lost in multiple different angiosperm line-
may not yet have been entirely enclosed by carpel ages. The early diverging angiosperm groups often
tissue, in the same way that the carpels of Amborella exhibit a perianth that shows gradual transition
are not fully closed (Dilcher 2000; Endress and Iger- from sepaloid outer organs to petaloid inner organs,
sheim 2000). The carpel tissue that had developed with no clear division point (discussed by Ronse de
would have enfolded individual groups of ovules, Craene et al. 2003). This morphology is facilitated
with the multiple fused carpels of many modern by their perianth phyllotaxy, which in many spe-
flowers still to evolve. cies is spiral and continuous, rather than discretely
The presence of small unisexual flowers with few whorled. This gradual transition of perianth organs
flower parts as well as large bisexual flowers with is shown by Amborella (Buzgo et al. 2004), the Nym-
many flower parts as fossils in deposits of similar phaeales (Warner et al. 2008), and some other early
ages has led to a range of suggestions as to the like- diverging groups.
ly morphology of the first flowers (Endress 1987). Differentiation of the perianth can in theory oc-
The larger fossil flowers are reminiscent of those cur either by modification of inner sepals to pro-
of modern-day Magnolia or waterlily, and both the duce petals, or by production of sterile stamens
Magnoliales and the Nymphaeales are early di- that evolve morphologically to produce petals. Both
verging groups. However, the smaller fossil flow- mechanisms have been shown to have occured in
ers resemble those of the Piperales (containing the different lineages, with a sepal-derived origin of
spice peppers). Interpretation of these fossil data petals usually postulated in early-diverging an-
is further complicated by the possibility that even giosperm groups and the monocots, but a stamen-
early fossil flowers had diverged from the ancestral derived origin of petals assumed for the eudicots.
morphology. For example, adaptation to an aquatic Some studies have assumed that the petals of the
lifestyle might change flower morphology consid- core eudicots (see Section 1.6) evolved only once,
erably, and many of the earliest angiosperm fossils from stamens, although recent reports have sug-
show clear evidence of an aquatic habit (Friis et al. gested that this is an over-simplification of a group
2001; Sun et al. 2002). which has itself experienced repeated petal loss
12   I N T R O D U C T I O N

and gain (Ronse de Craene 2007; Brockington et al. suite of novel colours, shapes, structures, scents,
2012). The molecular genetic basis of these various and rewards. At the same time, animal pollination
evolutions of the differentiated perianth probably is more likely than abiotic pollination to result in
involves similar homeotic mutations to those that reproductive isolation, particularly where specific
generated the bisexual reproductive shoot. The mo- pollinating animals are attracted only to a subset of
lecular basis of perianth morphology will be dis- floral attributes but the wind is random in its dis-
cussed for several examples in Chapter 11. persal of pollen. Such reproductive isolation may
have facilitated speciation and divergence of form,
further increasing the speed of angiosperm radia-
1.4 Floral diversification
tion. Finally, full closure of the carpel and the ability
The first angiosperm flowers were borne by a lin- to recognize and reject self pollen through biologi-
eage that subsequently underwent a dramatic ra- cal means may have evolved in concert to reinforce
diation, including an astonishing diversification outcrossing (Dilcher 2000).
of floral form. It has been hypothesized that this That rapid evolution coincided with the recruit-
process was initiated by the association of male and ment of animal pollinators is not in doubt, with
female organs on the same axis, which increased the the advantages of outcrossing and the ability to ex-
effectiveness of animal pollination (previously less change genetic information between widely spaced
significant than wind pollination for most plant spe- individuals representing major benefits in terms of
cies). An alternative hypothesis is that the appear- increased genetic diversity and thus ‘evolvability’.
ance of coloured pigments in the new flowers had What is less clear is the extent to which angiosperm
a dramatic effect on their attractiveness to animals, and flower radiation can be directly attributed to a
again establishing biotic pollination as the norm. subsequent coevolution between angiosperms and
Studies of the colour vision of a range of arthropods pollinating insects. This attractive hypothesis has
have inferred that the Cambrian ancestors of today’s informed much of pollination ecology for decades,
insects possessed the same trichromatic colour per- and can best be summarized by viewing flowers
ception system as that used by modern pollinating with a perianth as an angiosperm’s way of manipu-
insects to discriminate between flowers (Chittka lating an insect into carrying its pollen around for
1996). If insects were pre-adapted for viewing flow- it. Once the flower has acquired the ability to ma-
er colour 500 million years ago, then the appearance nipulate one insect, it may radiate (genetic variabil-
of coloured pigments in the perianth organs of the ity permitting) into as many different forms as there
first flowers may have rapidly led to a strong asso- are insects with different preferences to manipulate.
ciation between flowers and animal pollinators. In- There is some fossil evidence to support the hy-
creased animal pollination is likely to have resulted pothesis that angiosperm radiation was the result
in increased outcrossing, in part through the dual of angiosperm–insect coevolution. Fossils of early
service provided by an animal in both removing Cretaceous flowers show some features indicative
pollen from the anthers and applying non-self pol- of animal pollination, including a larger size than
len to the stigma of a single flower in a single visit. necessary for wind pollination (Crane et al. 1995).
This increase in outcrossing will have increased the The first Lepidoptera (butterflies and moths) ap-
amount of recombination between plant genomes pear in the fossil record at the same time as the
and therefore the speed of angiosperm evolution first angiosperms, and some groups of the Hy-
(Dilcher 2000). Outcrossing can be both advan- menoptera (bees, wasps, and ants) also appear to
tageous and disadvantageous to plants, having have evolved at the same time. However, there is
consequences for the genetic make-up of popula- little correlation between the origin or speciation of
tions and effective population size (Barrett 2002; other insect groups and the origin and speciation of
Charlesworth 2006; see also Chapter 13). However, the angiosperms (Willis and McElwain 2002). This
in many situations, selection will strongly favour suggests that angiosperm–insect coevolution may
adaptations that maintain increased outcrossing, have played an important role in the great diver-
resulting in the appearance and maintenance of a sification of some groups and floral forms, but that
 T he evolution of flowers    13

a significant part of this radiation must instead be 1.6 An introduction to angiosperm

attributed to the short lifespans and high rates of phylogeny
outcrossing of the new plants, and their consequent
rapid acquisition of new habitats and new niches. Throughout this book, reference will be made to
many different angiosperm species. In many cases
the aim will be to allow the reader to make com-
1.5 Morphological diversity of the flower parisons between species, or to draw evolutionary
The radiation of the angiosperms has resulted in conclusions. To allow ready access to a skeleton an-
a tremendous variety of floral form. This variety giosperm phylogeny, this section and the associated
encompasses size, shape, symmetry, organ num- Fig. 1.5 provide an overview of current thinking on
ber, whorl number, phyllotaxis, organ elaboration, relationships of different groups of flowering plants.
colour, pigmentation pattern, texture, scent, and This summary is based on the work of the Angio-
reward availability. The ecological and evolution- sperm Phylogeny Group (APG), and the phylog-
ary explanations for this variety are discussed in eny published as APG III (Angiosperm Phylogeny
Section III of this book, while its molecular genetic Group 2009). The APG is an informal collaboration
basis is discussed within Sections II and III (notably of plant systematists from several different coun-
Chapters 11, 15, 16, 17, and 18). However, it is worth tries, who work together to update and publish a
noting at this point that this diversity is not even- holistic picture of the whole angiosperm phylogeny,
ly distributed across the angiosperm phylogeny. often incorporating detailed data on specific groups
While the eudicot group contains by far the greatest contributed by other plant systematists. Their phy-
species diversity, estimated at around 70% of angio- logeny has come to be regarded as the most reliable
sperm species, its floral diversity is restricted to the reference point for angiosperm relationships.
details rather than the body plan of the whole flow- The phylogeny presented in Fig. 1.5 is based
er. Eudicot flowers generally have a whorled phyl- on orders of plants. Within each of these orders
lotaxis, differentiated perianth, and floral organs in are variable numbers of families. Throughout this
groups of five (although there are deviations from book, species will be described at first mention in
this basic pattern). Their diversity is at the level of a chapter, with their order in brackets following
size, symmetry, organ elaboration, colour, texture, the species name. The two exceptions to this rule
and scent. The monocots also have whorled phyl- are the molecular genetic models Arabidopsis thali-
lotaxis, with floral organs in groups of three. They ana (Brassicales) and Antirrhinum majus (Lamiales),
usually produce an undifferentiated perianth with which are discussed in almost every chapter and
two whorls of brightly coloured tepals, or else have are introduced in detail at first mention. Readers
dramatically modified wind-pollinated flowers who are interested in more detailed phylogeny can
such as those of the grasses (Poales). It is in the early find family relationships within each of the orders
diverging angiosperm groups, where species diver- on the Angiosperm Phylogeny Website (<www.
sity is only a few per cent of the angiosperm total, mobot.org/mobot/research/apweb>), along with
that the greatest diversity in floral body plan occurs. updates to the phylogeny as they occur.
As noted earlier, species in these groups have spi- At the base of the angiosperm phylogeny are a
ral, whorled, or transitional phyllotaxis. They show set of three sequentially branching orders, known
great variation in organ number, as well as diversity together as the early diverging angiosperms. The
of colour, scent, and floral elaboration. There is vari- Amborellales, at the base of the tree, contains only
ation in the shape of their ovules and carpels, and Amborella trichopoda, described above (see Sec-
in the degree to which the carpels are fully closed. tion 1.1.2) and now much studied as the earliest
It is likely that the relatively more constrained form diverging extant angiosperm. The Nymphaeales
of the eudicot flower has facilitated greater species contains the waterlilies, and the Austrobailey-
diversification by establishing a successful and flex- ales is a group of mainly tropical shrubs. After
ible floral form that is subject to variable selection these three orders, the phylogeny branches into
pressures from different pollinators. three points. The group known as the ­Magnoliids
14   I N T R O D U C T I O N

Dipsacales
Paracryphiales
Apiales
Bruniales
Escalloniales
Asterales
Aquifoliales
Boraginales
Solanales
Asterids Lamiales
Gentianales
Garryales
Ericales
Cornales
Caryophyllales
Berberidopsidales
Santalales
Brassicales
Malvales
Huertaeales
Sapindales Core eudicots
Picramniales
Crossosomatales
Myrtales
Rosids Geraniales
Fagales
Cucurbitales
Core eudicots
Rosales
Fabales
Malpighiales
Oxalidales
Celastrales
Zygophyllales
Vitales
Saxifragales
Dilleniaceae
Gunnerales
Eudicots Buxales
Trochodendrales
Sabiales
Proteales
Ranunculales
Ceratophyllales
Zingiberales
Commelinales
Poales
Arecales
Asparagales
Liliales Monocots
Pandanales
Dioscoreales
Petrosaviales
Alismatales
Acorales
Magnoliales
Laurales
Canellales Magnoliid
Piperales
Chloranthales
Austrobaileyales
Nymphaeales Early diverging
Amborellales

Figure 1.5 A summary of angiosperm phylogeny, based on APG III (Angiosperm Phylogeny Group 2009).
 T he evolution of flowers    15

contains the Magnoliales, Laurales, Canellales, eudicots, including the Ranunculales (buttercup
Piperales, and possibly the Chloranthales (which family), precede the branching of the Core Eud-
are sometimes excluded from the rest of the group). icots. The Core Eudicots contains many orders,
Many of these orders contain flowers that appear some branching independently but most contained
primitive, or show features in common with the within the Rosids or the Asterids. Important groups
early diverging angiosperms, but it is not clear within the Rosids include the Fabales (containing
whether these traits are ancestral or secondarily key model and crop legumes, such as pea, soybean,
derived. The Monocots are a very important group, and Medicago truncatula), the Malvales (cotton), and
containing 11 orders, including the economically the Brassicales (vegetable brassicas and the main
important Poales (the grasses). Within this order are genetic model, Arabidopsis thaliana). The Asterids
many important model and crop species, including also contains important orders, notably the Aster-
maize, rice, and wheat. The Liliales contains many ales (the species-rich daisies, including sunflower),
horticulturally important species, such as lily, tu- the Solanales (including potato, tomato, and au-
lip, and freesia, while the Asparagales contains bergine), and the Lamiales (containing the genetic
the enormously speciose orchid family. The third model Antirrhinum majus).
branch contains the Ceratophyllales and the Eud- For a thorough treatment of the diversity of the
icots. The Eudicots are the most species-rich section flowering plants in a phylogenetic context I recom-
of the tree, representing around 70% of angiosperm mend the books of Soltis et al. (2005) and Judd et al.
species diversity. Five orders of early diverging (2007).
 CH A PT ER 2

Historical interpretations of flower

induction and flower development

The modern analysis of flowers and flowering plants (translated and discussed by Arber 1946), in
rests on a wealth of literature concerned with the which he proposed that all plant organs could be
description and interpretation of plant form. Chief thought of as equivalent or analogous to a single
among these works is Goethe’s foliar theory, which type organ, which he called the leaf. However, it is
proposes that all aerial plant organs are analogous important to establish that he was not proposing a
to a single organ, which he calls the leaf. The foliar developmental or evolutionary concept, with other
theory has underpinned all work on flower devel- plant organs being descended from a leaf. Indeed,
opment, including modern molecular genetic anal- it might have helped to separate his thinking on
yses, as well as providing a frame of reference for equivalence from later evolutionary thinking on
evolutionary studies. This chapter describes Goe- relatedness if he had used a different name for his
the’s theory with reference to the flower, and its use hypothetical type organ. Nageli (1884) suggested
and expansion by twentieth-century botanists. An ‘phyllome’ as a more suitable name, a suggestion
analysis of the differences and similarities between with which later morphological botanists such as
vegetative and floral organs is presented, providing Arber (1937) strongly concurred. Because Goethe’s
a framework for a section that interprets the foliar theory implied no developmental or evolutionary
theory in an evolutionary context. The second half progression, it is effectively reciprocal. Thus it is
of the chapter moves on to consider historical inter- just as easy to describe leaves as analogous to petals
pretations of the transition from the vegetative state as it is to describe petals as analogous to leaves. In
to the flowering state, describing the mechanisms essence, Goethe’s view was that reproduction (and
proposed by early plant physiologists to explain the development of reproductive organs) ought to
this transition. Again, this overview is designed be treated as a function of the entire plant, and that
to provide context for further chapters on the cur- the flowering shoot could not be understood except
rent state of knowledge with regard to this floral in relation to the vegetative shoot of the same plant
transition. (Arber 1937). This holistic approach was a new de-
velopment in a field that had previously relied on
analysis of individual components of organisms. Its
genius lay in the detail with which it compared dif-
2.1 The foliar theory of the flower
ferent parts of the same plant, combined with the
The scientific study of plant morphology, and in simplicity of its approach. This approach involved
particular the study of comparative morphology, no speculation about the meaning behind the anal-
both of different organs within a plant and of the ogy of different plant organs. It provided, however,
same organ from different plants, was effectively a data set, free of preconceptions, which was then
the invention of the great German philosopher Jo- adopted by later evolutionary and developmental
hann Wolfgang von Goethe. In 1790, Goethe pub- biologists and has provided remarkable support for
lished his seminal essay on the metamorphosis of their theories.

Understanding Flowers and Flowering. Second Edition. Beverley Glover.

© Beverley Glover 2014. Published 2014 by Oxford University Press.
 H istorical interpretations    17

(a) (b)

(c) (d)

Figure 2.1 Analogous floral and

(e) reproductive organs in tobacco (Nicotiana
tabacum, Solanales). (a) The inflorescence
shoot (left) is analogous to the vegetative
shoot (right). (b) The bract (below) is
analogous to the leaf (above). (c) The sepal
(below) is analogous to the leaf (above).
(d) The petal (below) is analogous to the leaf
(above). (e) The stamen (below) is analogous
to the leaf (above).

Goethe’s analysis of the equivalence of the differ- usually remains indeterminate in the inflorescence
ent plant organs to a basic vegetative unit was sum- shoot, allowing indeterminate growth similar to
marized by Arber (1937), from which the following that shown previously by the vegetative shoot.
analysis of each of the reproductive structures is de- The inflorescence shoot’s direction of growth and
rived and expanded. Pairs of analogous structures its function—the production and support of lateral
are shown in Fig. 2.1. organs—are also the same as those of the vegetative
shoot.
Differences between the inflorescence shoot and
2.1.1 Inflorescence shoot
the vegetative shoot are primarily related to the
The inflorescence shoot consists of the shoot api- organs that they produce, and these will be con-
cal meristem (SAM), the stem which is laid down sidered individually below. However, within the
from the rib meristematic region of the SAM, and shoot itself a number of changes may occur. First,
the bracts, flowers, and secondary branches that are in some species, phyllotaxy in the inflorescence
produced laterally from that stem. Its similarities to shoot is altered, with organs being produced in a
the vegetative stem from which it derives are clear. pattern different from that of the vegetative shoot.
There is little difficulty in accepting such similari- Secondly, the distance between lateral organs may
ties, as the two are merely different phases in the vary. In many species the inflorescence shoot is
life cycle of the SAM, which itself undergoes no characterized by internodes shorter than those of
major reorganization of structure in the transition the vegetative shoot. Finally, the details of cellular
from the vegetative to the flowering stage, although differentiation within the epidermis of the stem
many changes in patterns of gene expression with- itself may be altered. For example, the vegetative
in that structure have been observed. The SAM stem of Antirrhinum majus (snapdragon, Lamiales)
18   I N T R O D U C T I O N

is entirely hairless, but the inflorescence stem is cov- in the floral shoot can therefore be thought of as
ered with short multicellular trichomes with glan- a ­reversion by the axis to a more juvenile growth
dular heads. form. Such retention of juvenile characteristics in
mature organisms is termed neoteny, and has been
hypothesized to be responsible for many apparent
saltational leaps in the animal fossil record, includ-
2.1.2 Floral shoot
ing the divergence of humans from apes. It is also
The floral shoot consists of the floral meristem and well known in plants, where it can be responsible
the lateral organs derived from it. It should not be for significant morphological evolution—for exam-
considered analogous to the main vegetative shoot ple, in floral form (Box et al. 2008; Box and Glover
(derived directly from the SAM) but to the axillary 2010). A third, and equally significant, difference
shoots which develop from the flanks of the SAM. between the flowering shoot and a vegetative shoot
In the same way, the floral meristems develop on is the determinacy of the meristem and consequent-
the flanks of the inflorescence meristem. The floral ly of the shoot. The early morphologists were con-
shoot usually arises in the axil of a leaf-like organ, cerned with the fate of the meristematic cells within
the bract, whereas the axillary vegetative shoot al- a flower, believing that consumption of the meris-
ways arises in the axil of a leaf. So the architecture tem by the terminal organs (the carpels) would indi-
of the floral shoot, and its positioning with respect cate a significant difference from the activity of the
to the main axis of plant growth, is very similar to axillary shoot. However, careful analysis has shown
that of a vegetative axillary shoot. The function of that many species retain an apex to the floral axis,
the floral shoot is also analogous—the production clearly distinct from the floral organs (see Fig. 2.2;
and support of lateral organs. Arber 1937). Instead of consumption by the carpels,
However, the differences between the floral shoot then, the floral meristem is simply determinate and
and an axillary vegetative shoot are not solely re- ceases to produce more organs a­ fter the flower is
stricted to the organs that they produce, very differ-
ent though those may seem. There are again three
significant differences between the floral shoot and a
vegetative shoot. First, phyllotaxy is almost always
altered in the floral shoot, with whorled phyllotaxy
being the norm in flower development (with nota-
ble exceptions), irrespective of the usual phyllotaxy
adopted by the leaves of the plant. Secondly, and
more significantly, there is an enormous difference
in the extent to which the shoot elongates. The axis
of a vegetative shoot will almost always elongate,
so that the leaves are separated by well-defined
internodes. In contrast, the floral axis very rarely
elongates at all after the production of the first se-
pal, producing organs so closely placed that fusions
both within and between different whorls of floral
organs are common. This difference was noted by
Goethe, and has been described as the primary di-
vergence between floral and vegetative shoots (Ar-
ber 1937). However, there are examples of primary
vegetative shoots adopting a similar form—many
species (e.g. in the Brassicales) adopt a rosette form Figure 2.2 The shoot apical meristem still present between the
in the juvenile phase, with almost no internodal carpels in a flower of Ranunculus acris (Ranunculales) (redrawn from
elongation at all. The loss of internodal expansion Arber 1937).
 H istorical interpretations    19

complete. It is likely that this determinacy, unusual 2.1.3 Bracts

in a plant meristem, is secondarily imposed. Genet-
If the evidence suggests that the vegetative and
ic analyses have revealed that floral meristem deter-
reproductive shoots are analogous, the various
minacy can be broken by mutation of a single gene
appendages borne by these shoots are increas-
(called AGAMOUS in Arabidopsis thaliana; Coen and
ingly difficult to relate to one another. The bract is
Meyerowitz 1991) and the meristem returned to an
the easiest case, being positionally and morpho-
indeterminate state (see Fig. 2.3). The analogy be-
logically often barely distinguishable from a leaf.
tween floral and vegetative meristems is therefore
Bracts, like leaves, are lateral organs produced by
not broken by the determinacy of the floral meris-
the SAM and which subtend a meristem. They
tem, a secondarily imposed character controlled by
are also in possession of dorsoventrality, are usu-
a single gene.
ally laminate in form, and are frequently green and
photosynthetic.
The differences between bracts and leaves are
(a) usually limited to details of size, shape, pigmenta-
tion, and cellular differentiation, although there are
some species in which bracts are entirely absent. In
many species the bracts are smaller than the foli-
age leaves, perhaps reflecting the transition of the
plant from an organism primarily concerned with
photosynthetic production to an organism con-
cerned with investing the products of that photo-
synthesis in reproduction. In some plants the bracts
have become modified to attract pollinators to the
flowers, and may therefore contain anthocyanin or
other pigments, either as well as or at the expense of
chlorophyll. Similarly, plants that use their bracts in
this way, such as some species of Cornus (Cornales),
may develop light-focusing papillae on their bracts
(b)
(Kay et al. 1981), while other species may show dif-
ferent trichome distributions on their bracts relative
to their leaves.

2.1.4 Sepals
The first whorl of perianth organs, containing the
sepals, is often morphologically very similar to a
whorl of leaves. The sepals are produced as lateral
appendages from the floral meristem, and are usu-
ally laminate in form and green in colour. Excep-
tions to this occur in species where both whorls
of perianth organs are specialized for pollinator
attraction, either as two very similar whorls, such
as in the Liliales, or as two very different whorls,
Figure 2.3 The indeterminate nature of the AGAMOUS mutant such as in Fuchsia (Myrtales). In both cases the two
flower (b), which produces flowers within flowers, confirms that
determinacy has been imposed upon the wild type floral meristem
whorls of petaloid organs are sometimes known
(a) by the action of this single gene. Photographs kindly supplied by as tepals. Apart from this particular difference,
Ian Furner (University of Cambridge). related to adoption of a novel function, the sepals
20   I N T R O D U C T I O N

usually differ from leaves only in their size, often 2.1.6 Stamens
being much smaller.
The outer whorl of reproductive organs, the sta-
mens, was also considered analogous to leaves by
2.1.5 Petals Goethe. The similarities of stamens to leaves lie
in the presence of chlorophyll and in their growth
The second whorl of perianth organs can, in species
form, which consists of elongation in a single plane
with a simple undifferentiated perianth, be mor-
(although usually with little or no laminar growth).
phologically very similar to leaves, too. However,
Their differences may seem more striking, but can
in many species, particularly in some of the eud-
again be attributed to minor adaptations to chang-
icots with zygomorphic (or bilaterally symmetrical)
ing function. The absence of a laminar form may
flowers, the petals can be morphologically very dis-
at first seem significant. However, analysis of mu-
tinct both from leaves and from one another. How-
tants with perturbations in leaf development has
ever great the differences in morphology between
shown that, in order for a leaf to develop a lamina,
petals and leaves may seem, they are nonetheless
it must first have dorsoventrality (Waites and Hud-
analogous in terms of their position as lateral ap-
son 2001). Put simply, a leaf cannot grow sideways
pendages from a meristem. Other similarities in-
unless it can detect which way is up, which way is
clude dorsoventrality and a laminar form. Both
down, and thus which way is sideways. There is no
petals and leaves can clearly be seen to distinguish
need for a stamen to have dorsoventrality, as it is
their dorsal surface from their ventral surface. The
simply a filament supporting the pollen-containing
leaves of most angiosperm species differentiate sto-
locules. In the absence of dorsoventrality a laminar
mata at a considerably higher frequency on their
form cannot develop, so the lack of a lamina can
ventral epidermis than on their dorsal epidermis.
be interpreted as a consequence of the loss of dor-
Internally, the palisade mesophyll (the columnar
soventrality. That leaves the locules themselves as
cells that provide the extended surface area for
the only significant difference between stamens and
photosynthesis) is located on the dorsal side of the
leaves.
leaf. Similarly, many petals develop specialized epi-
A further argument in favour of the analogy be-
dermal cells on their dorsal surfaces, and may even
tween leaves and stamens is the interrelationship
be differentially pigmented or patterned on their
between petals and stamens. A variety of authors,
dorsal and ventral surfaces. The laminar form, pro-
beginning with Goethe himself, observed significant
duced by growth perpendicular to an initial axis, is
similarities between stamens and petals. It had also
also common to both leaves and petals.
been noted that the absence of stamens in species
If the similarities between petals and leaves are
which produce some female-only flowers was often
in major architectural and developmental charac-
associated with a reduction in petal development.
teristics, the differences are largely in the detail of
Modern molecular genetic analyses have ­confirmed
function. Petals are not usually green and photosyn-
the association between petals and stamens, with
thetic, but instead may contain pigments that make
both requiring the activity of ‘­ B-function’ genes
them stand out against vegetation. This can be in-
(see Chapter 10) for their development (Coen and
terpreted as a secondary adaptation to their specific
Meyerowitz 1991). It follows, then, that if petals are
function as pollinator attractants. Similarly, petals
analogous to leaves, and petals and stamens are
usually have no palisade mesophyll (since they do
variations on the same theme, then stamens must
not photosynthesize), and often develop elaborate
also be analogous to leaves.
papillate epidermal cells to enhance their apparent
colour and texture. These differences, like changes
in size and shape, do not reflect major differences
2.1.7 Carpels
between petals and leaves, but rather minor modi-
fications of a similar ground plan, and therefore do The female reproductive structures have tradition-
not perturb Goethe’s vision of the analogous nature ally presented the greatest difficulty to people in-
of leaves and petals. tent on interpreting the flower in a foliar context.
 H I S TO R I C A L I N T E R P R E TAT I O N S 21

Single fused Three fused

carpel carpels
Sporangia

Modified leaf

Figure 2.4 Development of the angiosperm

carpel. A modified leaf with sporangia at the
edges folds up to make a single fused carpel,
several of which may fuse together in a
single gynoecium.

Goethe himself had some difficulties with the car- make up a flower look as if they could be produced
pel, and it was not until microscopical techniques with only a few variations using the same basic de-
advanced considerably that it was possible to see velopmental programmes that make leaves. Flow-
how the development of each carpel was analogous ers, in fact, seem to be nothing more than bunches
to the development of a leaf. Each carpel is essen- of slightly strange leaves bearing spore-producing
tially composed of a folded up leaf-like structure, structures.
with ovules developing on its adaxial side (see
Fig. 2.4). In most species, multiple carpels fuse to-
gether to form a single compound pistil. Ovules 2.2 The foliar theory in an evolutionary
aside, the only differences between carpels and
context
leaves are the development of specialized stigmatic
cells and the patterning of the vasculature. The stig- The observations of Goethe on the analogous na-
matic cells, and the stylar tissue beneath them, are ture of leaves and floral organs paved the way for
clearly adaptations to the function of the carpel, and later evolutionary interpretations of flower devel-
can be interpreted as secondary consequences of the opment. Where organs can be seen to represent
novel function. The significance of the patterning of variations on a theme, it is only a short step to blur
carpel vasculature has been the subject of much de- the boundaries between them and imagine inter-
bate in the literature. The essential problem is that mediate forms. This ‘fuzzy’ approach to plant mor-
leaves have a dominant mid-vein with secondary phology (Rutishauser and Isler 2001) fits perfectly
vasculature branching outwards from it, whereas with the idea, propounded by Darwin, that organ-
carpels have dominant lateral veins with secondary isms were formed by gradual transitions between
veins branching inwards from them. Although it is types. Goethe’s work provided important data
not clear how the distribution of vasculature could that supported the theory of evolution by natural
have altered, it has generally come to be accepted selection, suggesting that the various organs of the
that this pattern reflects the lateral positions of the flower evolved by gradual changes, as a result of
ovules, and the need to supply them with nutrients, mutations, from an ancestral leaf-like structure.
and is thus likely to be a secondary consequence of As evolutionary theory became accepted as part of
ovule development. mainstream biology, Goethe’s ideas were seamless-
Overall, then, comparative morphology shows us ly incorporated into an evolutionary context, with
that Goethe’s foliar theory of the flower was both his cautious ‘analogous’ converted to a more radical
innovative and insightful. All of the organs that ‘related to’ or ‘derived from.’
22   I N T R O D U C T I O N

The idea that floral organs are only a few muta- flower by grafting a single induced leaf from anoth-
tions different from leaves has been the founda- er plant on to it. It is clear from this physical separa-
tion stone of modern molecular genetic analysis of tion of processes that floral evocation requires the
flower development. Genetic analysis in the 1980s production of a signal by the induced organs, which
and 1990s identified lines of plants with mutations is transported to the apical meristem and activates
that caused interconversion of floral organs. Com- flower production. The mechanisms of induction
bination of these mutations into a single plant line and evocation, and the nature of the signal between
resulted in a plant that produced four whorls of them, have long been the subjects of physiological
leaves in place of the four whorls of floral organs, analysis.
finally providing the molecular ‘proof’ for Goethe’s
foliar theory (Coen and Meyerowitz 1991). These 2.4 Developmental explanations
mutant lines, and the genes in question, are dis-
of floral induction
cussed in more detail in Chapter 10. However, their
interpretation, and indeed much of the impetus for The variables that interact to determine when a
their identification, rely heavily on the historical plant is induced to flower can include develop-
work of Goethe himself. mental stimuli and environmental stimuli. For the
majority of plants in temperate climates the envi-
ronment is a key factor in the decision to flower,
2.3 The transition to flowering
as producing vulnerable flowers and seeds in the
The history of scientific work on flower develop- depths of winter, for example, would not be a suc-
ment may belong to comparative morphologists, cessful strategy. For this reason, environmental
but the history of work on the transition to flower- stimuli are considered in much greater depth than
ing lies with plant physiologists. The transition to developmental ones, both in this chapter and in the
flowering consists of a major phase change in the literature as a whole. Developmental factors are of
plant’s life cycle. A plant that has previously pro- more importance to plants living in environments
duced only leaves and axillary meristems from its with little annual variation. It is unusual, for in-
apical meristem must now switch to producing stance, to find a tropical forest species with a floral
bracts and floral meristems, along with any chang- transition determined by factors such as day length
es to the general axis, phyllotaxy, and pattern of or temperature, which are more or less constant in
growth. This switch can be thought of as a ‘deci- that environment.
sion’ on the part of the plant—it is not a random The developmental factors that may influence the
event, but occurs in response to one or several of a floral transition generally refer to the age and health
large set of potential stimuli, which vary from spe- of the plant. Some trees, for example, can only
cies to species. The transition to flowering can be flower after a certain number of years of growth.
broken down into two distinct processes, induction This ensures that the tree has had time to build up
and evocation. Floral induction is the commitment a store of photosynthate with which to support any
of the plant to start producing flowers, which often developing seeds and fruit. Similarly, some herba-
happens as a result of processes occurring in the ceous and weedy species flower after the produc-
leaves. Once induced, a plant is set on the path to tion of a certain number of leaves, again allowing
flowering, even though no flowers have yet been for the development of sufficient photosynthetic
produced. The induced plant then evokes the pro- tissue to support the nutritional needs of non-
duction of flowers by triggering changes in gene photosynthetic flowers, seed, and fruit (King 1997).
expression in the apical meristem. Induction and Although the human observer might interpret these
evocation are usually considered separately for the responses as implying a ‘counting’ mechanism
simple reason that they often occur in distinct or- within the plant, it is more likely that each leaf pro-
gans. It is possible to induce many plants to flower duces a certain amount of a stimulatory substance,
by providing appropriate stimuli to a single leaf, and that the ‘right’ number of leaves are required
and it is possible to evoke an uninduced plant to to produce sufficient stimulus to cross a threshold,
Exploring the Variety of Random
Documents with Different Content
 Pues por llevar los despojos
De todos cuantos te ven,
Haces, ó niña, que estén
Los hechizos en tus ojos.
En sus fuerzas te adelantas,
Pues bailando nos admiras,
Y nos matas, si nos miras,
Y nos encantas, si cantas.
De cien mil modos hechizas,
Hables, calles, cantes, mires,
Ó te acerques ó retires,
El fuego de amor atizas.
Sobre el mas exento pecho
Tienes mando y señorío;
De lo que es testigo el mio,
De tu imperio satisfecho.
Preciosa joya de amor,
Esto humildemente escribe
El que por tí muere y vive
Pobre, aunque humilde amador.
—En pobre acaba el último verso, dijo á esta sazon Preciosa, mala
señal; nunca los enamorados han de decir que son pobres, porque á
los principios á mi parecer la pobreza es muy enemiga del amor.
—¿Quién te enseña eso, rapaza? dijo uno.
—¿Quién me lo ha de enseñar? respondió Preciosa; ¿no tengo yo
mi alma en mi cuerpo? ¿no tengo ya quince años? No soy manca, ni
ronca, ni estropeada del entendimiento: los ingenios de las jitanas
van por otro norte que los de las demas gentes; siempre se
adelantan á sus años, no hay jitano necio, ni jitana lerda; que como
el sustentar su vida consiste en ser agudos, astutos y embusteros,
despabilan el ingenio á cada paso, y no dejan que crie moho en
ninguna manera. ¿Ven estas muchachas mis compañeras, que están
callando, y parecen bobas? pues éntrenles el dedo en la boca, y
tiéntenlas las cordales, y verán lo que verán: no hay muchacha de
doce que no sepa lo que de veinticinco, porque tienen por maestros
y preceptores al diablo y al uso, que les enseña en una hora lo que
habian de aprender en un año.
Con esto que la Jitanilla decia, tenia suspensos á los oyentes, y
los que jugaban le dieron barato, y aun los que no jugaban. Cogió la
hucha de la vieja treinta reales, y mas rica y mas alegre que una
pascua de flores, antecogió sus corderas, y fuese en casa del señor
tiniente, quedando que otro dia volveria con su manada á dar
contento á aquellos tan liberales señores.
Ya tenia aviso la señora Doña Clara, mujer del señor tiniente,
como habian de ir á su casa las jitanillas, y estábalas esperando
como agua de mayo ella y sus doncellas y dueñas, con las de otra
señora vecina suya, que todas se juntaron para ver á Preciosa; y
apénas hubieron entrado las jitanas, cuando entre las demas
resplandeció Preciosa, como la luz de una antorcha entre otras luces
menores; y así corrieron todas á ella: unas la abrazaban, otras la
miraban, estas la bendecian, aquellas la alababan. Doña Clara decia:
—Este sí que se puede decir cabello de oro, estos sí que son ojos
de esmeraldas.
La señora su vecina la desmenuzaba toda, y hacia pepitoria de
todos sus miembros y coyunturas; y llegando á alabar un pequeño
hoyo que Preciosa tenia en la barba, dijo:
—¡Ay qué hoyo! en este hoyo han de tropezar cuantos ojos le
miraren.
Oyó esto un escudero de brazo de la señora Doña Clara, que allí
estaba, de luenga barba y largos años, y dijo:
—¿Ese llama vuesa merced hoyo, señora mia? pues yo sé poco de
hoyos, ó ese no es hoyo, sino sepultura de deseos vivos: por Dios
tan linda es la Jitanilla, que hecha de plata ó de alcorza no podria
ser mejor. ¿Sabes decir la buenaventura, niña?
—De tres ó cuatro maneras, respondió Preciosa.
—Y ¿eso mas? dijo Doña Clara, por vida del tiniente mi señor, que
me la has de decir, niña de oro, y niña de plata, y niña de perlas, y
niña de carbunclos, y niña del cielo, que es lo mas que puedo decir.
—Denle, denle la palma de la mano á la niña, y con qué haga la
cruz, dijo la vieja, y verán qué de cosas les dice; que sabe mas que
un dotor de melecina.
 Echó mano á la faldriquera la señora tinienta, y halló que no tenia
blanca: pidió un cuarto á sus criadas, y ninguna le tuvo, ni la señora
vecina tampoco. Lo cual, visto por Preciosa, dijo:
—Todas las cruces en cuanto cruces son buenas; pero las de plata
ó de oro son mejores, y el señalar la cruz en la palma de la mano
con moneda de cobre, sepan vuesas mercedes que menoscaba la
buenaventura, por lo ménos la mia: y así tengo aficion á hacer la
cruz primera con algun escudo de oro, ó con algun real de á ocho, ó
á lo ménos de á cuatro; que soy como los sacristanes que cuando
hay buena ofrenda se regocijan.
—Donaire tienes, niña, por tu vida, dijo la señora vecina.
Y volviéndose al escudero le dijo:
—Vos, señor Contreras, ¿tendréis á mano algun real de á cuatro?
dádmele, que en viniendo el dotor mi marido os le volveré.
—Sí tengo, respondió Contreras, pero téngole empeñado en
veinte y dos maravedís que cené anoche: dénmelos, que yo iré por
él en volandas.
—No tenemos entre todas un cuarto, dijo Doña Clara, ¿y pedís
veinte y dos maravedís? Andad, Contreras, que siempre fuisteis
impertinente.
Una doncella de las presentes, viendo la esterilidad de la casa,
dijo á Preciosa:
—Niña, ¿hará algo al caso que se haga la cruz con un dedal de
plata? Antes, respondió Preciosa, se hacen las cruces mejores del
mundo con dedales de plata, como sean muchos.
—Uno tengo yo, replicó la doncella; si este basta, héle aquí, con
condicion que tambien se me ha de decir á mí la buenaventura.
—¡Por un dedal tantas buenasventuras! dijo la jitana vieja: nieta,
acaba presto, que se hace noche.
Tomó Preciosa el dedal, y la mano de la señora tinienta, y dijo:
 Hermosita, hermosita,
La de las manos de plata,
Mas te quiere tu marido
Que al rey de las Alpujarras.
Eres paloma sin hiel,
Pero á veces eres brava
Como leona de Oran,
Ó como tigre de Ocaña.
Pero en un tras, en un tris,
El enojo se te pasa,
Y quedas como alfeñique,
Ó como cordera mansa.
Riñes mucho, y comes poco;
Algo celosita andas;
Que es jugueton el tiniente,
Y quiere arrimar la vara.
Cuando doncella te quiso
Uno de una buena cara;
Que mal hayan los terceros
Que los gustos desbaratan.
Si á dicha tú fueras monja,
Hoy tu convento mandaras,
Porque tienes de abadesa
Mas de cuatrocientas rayas.
No te lo quiero decir,
Pero poco importa, vaya,
Enviudarás otra vez,
Y otras dos serás casada.
No llores, señora mia,
Que no siempre las jitanas
Decimos el Evangelio;
No llores, señora, acaba.
Como te mueras primero
Que el señor tiniente, basta
Para remediar el daño
De la viudez que amenaza.
 Has de heredar y muy presto
Hacienda en mucha abundancia;
Tendrás un hijo canónigo,
La iglesia no se señala,
De Toledo no es posible.
Una hija rubia y blanca
Tendrás, que si es religiosa,
Tambien vendrá á ser prelada.
Si tu esposo no se muere
Dentro de cuatro semanas,
Verásle corregidor
De Búrgos ó Salamanca.
Un lunar tienes: ¡qué lindo!,
¡Ay Jesus, qué luna clara!
¡Qué sol, que allá en los antipodas
Escuros valles aclara!
Mas de dos ciegos por verle
Dieran mas de cuatro blancas:
Agora si es la risica;
¡Ay, que bien haya esa gracia!
Guárdate de las caidas,
Principalmente de espaldas;
Que suelen ser peligrosas
En las principales damas.
Cosas hay mas que decirte:
Si para el viérnes me aguardas,
Las oirás, que son de gusto,
Y algunas hay de desgracias.
Acabó su buenaventura Preciosa, y con ella encendió el deseo de
todas las circunstantes en querer saber la suya, y así se lo rogaron
todas; pero ella las remitió para el viérnes venidero, prometiéndole
que tendrian reales de plata para hacer las cruces.
En esto vino el señor tiniente, á quien contaron maravillas de la
Jitanilla: él las hizo bailar un poco, y confirmó por verdaderas y bien
dadas las alabanzas que á Preciosa habian dado: y poniendo la
mano en la faldriquera, hizo señal de querer darle algo; y habiéndola
espulgado y sacudido, y rascado muchas veces, al cabo sacó la
mano vacía, y dijo:
—Por Dios que no tengo blanca, dadle vos, doña Clara, un real á
Preciosica, que os le daré despues.
—Bueno es eso, señor, por cierto; sí, ahí está el real de
manifiesto: no hemos tenido entre todas nosotras un cuarto para
hacer la señal de la cruz, ¿y quiere que tengamos un real?
—Pues dadle alguna valoncica vuestra, ó alguna cosa, que otro
dia nos volverá á ver Preciosa, y la regalaremos mejor.
Á lo cual dijo Doña Clara:
—Pues porque otra vez venga, no quiero dar nada ahora á
Preciosa.
—Antes si no me dan nada, dijo Preciosa, nunca mas volveré acá:
mas, sí, volveré á servir á tan principales señores; pero traeré
tragado que no me han de dar nada, y ahorraréme la fatiga del
esperarlo. Coheche vuesa merced, señor tiniente, coheche y tendrá
dineros, y no haga usos nuevos, que morirá de hambre. Mire, señor;
por ahí he oido decir (y aunque moza, entiendo que no son buenos
dichos) que de los oficios se ha de sacar dineros para pagar las
condiciones de las residencias, y para pretender otros cargos.
—Así lo dicen y lo hacen los desalmados, replicó el tiniente; pero
el juez que da buena residencia, no tendrá que pagar condenacion
alguna, y el haber usado bien su oficio, será el valedor para que le
den otro.
—Habla vuesa merced muy á lo santo, señor tiniente, respondió
Preciosa; ándese á eso, y cortarémosle de los harapos para reliquias.
—Mucho sabes, Preciosa, dijo el tiniente: calla, que yo daré traza
que sus Majestades te vean, porque eres pieza de reyes.
—Querránme para truhana, respondió Preciosa, y yo no lo sabré
ser, y todo irá perdido; si me quisiesen para discreta, aun
llevarmeian; pero en algunos palacios mas medran los truhanes que
los discretos: yo me hallo bien con ser jitana y pobre, y corra la
suerte por donde el cielo quisiere.
—Ea, niña, dijo la jitana vieja, no hables mas, que has hablado
mucho, y sabes mas de lo que yo te he enseñado; no te asotiles
tanto, que te despuntarás: habla de aquello que tus años permiten,
y no te metas en altanerías, que no hay ninguna que no amenace
caida.
—El diablo tienen estas jitanas en el cuerpo, dijo á esta sazon el
tiniente.
Despidiéronse las jitanas, y al irse dijo la doncella del dedal:
—Preciosa, díme la buenaventura, ó vuélveme mi dedal, que no
me queda con que hacer labor.
—Señora doncella, respondió Preciosa, haga cuenta que se la he
dicho, y provéase de otro dedal, ó no haga vainillas hasta el viérnes,
que yo volveré, y le diré mas venturas y aventuras que las que tiene
un libro de caballerías.
Fuéronse, y juntáronse con las muchas labradoras que á la hora
de las Avemarías suelen salir de Madrid, para volverse á sus aldeas,
y entre otras vuelven muchas, con quien siempre se acompañaban
las jitanas, y volvian seguras; porque la jitana vieja vivia en continuo
temor no le salteasen á su Preciosa.
Sucedió pues que la mañana de un dia que volvian á Madrid á
coger la garrama con las demas jitanillas, en un valle pequeño que
está obra de quinientos pasos ántes que se llegue á la villa, vieron
un mancebo gallardo y ricamente aderezado de camino: la espada y
daga que traia eran, como decir se suele, un ascua de oro: sombrero
con rico cintillo, y con plumas de diversas colores adornado.
Repararon las jitanas en viéndole, y pusiéronsele á mirar muy
despacio, admiradas de que á tales horas un tan hermoso mancebo
estuviese en tal lugar á pié y solo. Él se llegó á ellas, y hablando con
la jitana mayor, le dijo:
—Por vida vuestra, amiga, que me hagais placer que vos y
Preciosa me oyais aquí aparte dos palabras, que serán de vuestro
provecho.
—Como no nos desviemos mucho, ni nos tardemos mucho, sea
en buen hora, respondió la vieja.
Y llamando á Preciosa, se desviaron de las otras obra de veinte
pasos, y así en pié como estaban, el mancebo les dijo:
—Yo vengo de manera rendido á la discrecion y belleza de
Preciosa, que despues de haberme hecho mucha fuerza para
escusar llegar á este punto, al cabo he quedado mas rendido, y mas
imposibilitado de escusallo. Yo, señoras mias (que siempre os he dar
este nombre, si el cielo mi pretension favorece), soy caballero, como
lo puede mostrar el hábito; y apartando el herreruelo, descubrió en
el pecho uno de los mas calificados que hay en España: soy hijo de
fulano (que por buenos respetos aquí no se declara su nombre),
estoy debajo de su tutela y amparo: soy hijo único, y el que espera
un razonable mayorazgo: mi padre está aquí en la corte
pretendiendo un cargo, y ya está consultado, y tiene casi ciertas
esperanzas de salir con él; y con ser de la calidad y nobleza que os
he referido, y de la que casi se os debe ya de ir trasluciendo, con
todo eso quisiera ser un gran señor para levantar á mi grandeza la
humildad de Preciosa, haciéndola mi igual y mi señora: yo no la
pretendo para burlalla, ni en las veras del amor que la tengo puede
caber género de burla alguna: solo quiero servirla del modo que ella
mas gustare: su voluntad es la mia; pero con ella es de cera mi
alma, donde podrá imprimir lo que quisiere, y para conservarlo y
guardarlo, no será como impreso en cera, sino como esculpido en
mármoles, cuya dureza se opone á la duracion de los tiempos: si
creeis esta verdad, no admitirá ningun desmayo mi esperanza; pero
si no me creeis, siempre me tendrá temeroso vuestra duda: mi
nombre es este, y díjoselo: el de mi padre ya os le he dicho: la casa
donde vive es en tal calle, y tiene tales y tales señas: vecinos tiene
de quien podréis informaros, y aun de los que no son vecinos
tambien; que no es tan escura la calidad y el nombre de mi padre, y
el mio, que no le sepan en los patios de Palacio, y aun en toda la
corte: cien escudos traigo aquí en oro para daros en arras y señal de
lo que pienso daros; porque no ha de negar la hacienda el que da el
alma.
En tanto que el caballero esto decia, le estaba mirando Preciosa
atentamente, y sin duda que no le debieron de parecer mal ni sus
razones ni su talle; y volviéndose á la vieja, le dijo:
—Perdóneme, abuela, de que me tome licencia para responder á
este tan enamorado señor.
—Responde lo que quisieres, nieta, respondió la vieja, que yo sé
que tienes discrecion para todo.
Y Preciosa dijo:
 —Yo, señor caballero, aunque soy jitana, pobre y humildemente
nacida, tengo un cierto espiritillo fantástico acá dentro, que á
grandes cosas me lleva: á mí ni me mueven promesas, ni me
desmoronan dádivas, ni me inclinan sumisiones, ni me espantan
finezas enamoradas: y aunque de quince años (que segun la cuenta
de mi abuela para este San Miguel los haré), soy ya vieja en los
pensamientos, y alcanzo mas de aquello que mi edad promete, mas
por mi buen natural que por la esperiencia; pero con lo uno ó con lo
otro sé que las pasiones amorosas en los recien enamorados son
como ímpetus indiscretos que hacen salir á la voluntad de sus
quicios, la cual atropellando inconvenientes, desatinadamente se
arroja tras su deseo, y pensando dar con la gloria de sus ojos, da
con el infierno de sus pesadumbres: si alcanza lo que desea,
mengua el deseo con la posesion de la cosa deseada, y quizá
abriéndose entónces los ojos del entendimiento, se ve ser bien que
se aborrezca lo que ántes se adoraba: este temor engendra en mí
un recato tal, que ningunas palabras creo, y de muchas obras dudo:
una sola joya tengo, que la estimo en mas que á la vida, que es la
de mi entereza y virginidad, y no la tengo de vender á precio de
promesas ni dádivas, porque en fin será vendida, y si puede ser
comprada, será de muy poca estima: ni me la han de llevar trazas ni
embelecos, ántes pienso irme con ella á la sepultura, y quizá al cielo,
que ponerla en peligro que quimeras y fantasías soñadas la
embistan ó manoseen: flor es la de la virginidad que á ser posible
aun con la imaginacion no habia de dejar ofenderse: cortada la rosa
del rosal, ¡con qué brevedad y facilidad se marchita! Este la toca,
aquel la huele, el otro la deshoja, y finalmente, entre las manos
rústicas se deshace: si vos, señor, por sola esta prenda venís, no la
habeis de llevar sino atada con las ligaduras y lazos del matrimonio;
que si la virginidad se ha de inclinar, ha de ser á este santo yugo,
que entónces no seria perderla, sino emplearla en ferias que felices
ganancias prometen: si quisiéredes ser mi esposo, yo lo seré
vuestra; pero han de proceder muchas condiciones y averiguaciones
primero: primero tengo de saber si sois el que decís: luego, hallando
esta verdad, habeis de dejar la casa de vuestros padres y la habeis
de trocar con nuestros ranchos, y tomando el traje de jitano, habeis
de cursar dos años en nuestras escuelas, en el cual tiempo me
satisfaré yo de vuestra condicion, y vos de la mia: al cabo del cual, si
vos os contentades de mí, y yo de vos, me entregaré por vuestra
esposa; pero hasta entónces tengo de ser vuestra hermana en el
trato, y vuestra esclava en serviros: y habeis de considerar que en el
tiempo deste noviciado podria ser que cobrásedes la vista, que
agora debeis de tener perdida, ó por lo ménos turbada, y viésedes
que os convenia huir de lo que agora seguís con tanto ahinco; y
cobrando la libertad perdida, con un buen arrepentimiento se
perdona cualquier culpa: si con estas condiciones quereis entrar á
ser soldado de nuestra milicia, en vuestra mano está, pues faltando
alguna dellas, no habeis de tocar un dedo de la mia.
Pasmóse el mozo á las razones de Preciosa, y púsose como
embelesado mirando al suelo, dando muestras que consideraba lo
que de responder debia. Viendo lo cual Preciosa, tornó á decirle:
—No es este caso de tan poco momento, que en los que aquí nos
ofrece el tiempo pueda ni deba resolverse: volvéos, señor, á la villa,
y considerad despacio lo que viéredes que mas os convenga, y en
este mismo lugar me podeis hablar todas las fiestas que quisiéredes,
al ir ó venir de Madrid.
Á lo cual respondió el gentil hombre:
—Cuando el cielo me dispuso para quererte, Preciosa mia,
determiné de hacer por tí cuanto tu voluntad acertase á pedirme,
aunque nunca cupo en mi pensamiento que me habias de pedir lo
que me pides; pero pues es tu gusto, que el mio al tuyo se ajuste y
acomode, cuéntame por jitano desde luego, y haz de mí todas las
esperiencias que mas quisieres, que siempre me has de hallar el
mismo que ahora te significo: mira cuándo quieres que mude el
traje, que yo queria que fuese luego, que con ocasion de ir á
Flándes engañaré á mis padres, y sacaré dineros para gastar
algunos dias, y serán hasta ocho los que podré tardar en acomodar
mi partida: á los que fueren conmigo, yo los sabré engañar de modo
que salga con mi determinacion; lo que te pido es, si es que ya
puedo tener atrevimiento de pedirte y suplicarte algo, que si no es
hoy donde te puedes informar de mi calidad y de la de mis padres,
que no vayas mas á Madrid, porque no querria que algunas de las
demasiadas ocasiones que allí pueden ofrecerse, me salteasen la
buena ventura que tanto me cuesta.
—Eso no, señor galan, respondió Preciosa: sepa que conmigo ha
de andar siempre la libertad desenfadada, sin que la ahogue ni turbe
la pesadumbre de los celos; y entienda que no la tomaré tan
demasiada que no se eche de ver desde bien léjos, que llega mi
honestidad á mi desenvoltura; y en el primero cargo en que quiero
enteraros, es en el de la confianza que habeis de hacer de mí: y
mirad que los amantes que entran pidiendo celos, ó son simples ó
confiados.
—Satanas tienes en tu pecho, muchacha, dijo á esta sazon la
jitana vieja: mira que dices cosas, que no las dirá un colegial de
Salamanca: tú sabes de amor, tú sabes de celos, tú de confianzas:
¿cómo es esto? que me tienes loca, y te estoy escuchando como á
una persona espiritada, que habla latin sin saberlo.
—Calle, abuela, respondió Preciosa, y sepa que todas las cosas
que me oye son nonadas, y son de burlas para las muchas que de
mas veras me quedan en el pecho.
Todo cuanto Preciosa decia, y toda la discrecion que mostraba,
era añadir leña al fuego que ardia en el pecho del enamorado
caballero. Finalmente, quedaron en que de allí á ocho dias se verian
en aquel mismo lugar, donde él vendria á dar cuenta del término en
que sus negocios estaban, y ellas habrian tenido tiempo de
informarse de la verdad que les habia dicho. Sacó el mozo una
bolsilla de brocado, donde dijo que iban cien escudos de oro, y
dióselos á la vieja; pero no queria Preciosa que los tomase en
ninguna manera, á quien la jitana dijo:
—Calla, niña, que la mejor señal que este señor ha dado de estar
rendido, es haber entregado las armas en señal de rendimiento; y el
dar, en cualquiera ocasion que sea, siempre fué indicio de generoso
pecho; y acuérdate de aquel refran que dice: al cielo rogando, y con
el mazo dando; y mas, que no quiero yo que por mí pierdan las
jitanas el nombre que por luengos siglos tienen adquirido de
codiciosas y aprovechadas: ¿cien escudos quieres tú que deseche,
Preciosa, que pueden andar cosidos en el alforza de una saya que
no valga dos reales, y tenerlos allí como quien tiene un juro sobre
las yerbas de Estremadura? Si alguno de nuestros hijos, nietos ó
parientes cayere por alguna desgracia en manos de la justicia,
¿habrá favor tan bueno que llegue á la oreja del juez y del
escribano, como estos escudos, si llegan á sus bolsas? Tres veces
por tres delitos diferentes me he visto casi puesta en el asno, para
ser azotada; y de la una me libró un jarro de plata, y de la otra una
sarta de perlas, y de la otra cuarenta reales de á ocho, que habia
trocado por cuartos, dando veinte reales mas por el cambio: mira,
niña, que andamos en oficio muy peligroso y lleno de tropiezos y de
ocasiones forzosas, y no hay defensas que mas presto nos amparen
y socorran, como las armas invencibles del gran Filipo: no hay pasar
adelante de su plus ultra: por un doblon de dos caras se nos
muestra alegre la triste del procurador y de todos los ministros de la
muerte, que son arpías de nosotras las pobres jitanas, y mas precian
pelarnos y desollarnos á nosotras, que á un salteador de caminos:
jamas por mas rotas y desastradas que nos vean, nos tienen por
pobres, que dicen que somos como los jubones de los gabachos de
Belmonte, rotos y grasientos, y llenos de doblones.
—Por vida suya, abuela, que no diga mas, que lleva término de
alegar tantas leyes en favor de quedarse con el dinero, que agote las
de los emperadores: quédese con ellos, y buen provecho le hagan, y
plega á Dios que los entierre en sepultura donde jamas tornen á ver
la claridad del sol, ni haya necesidad que le vean: á estas nuestras
compañeras será forzoso darles algo, que ha mucho que nos
esperan, y ya deben estar enfadadas.
—Así verán ellas, replicó la vieja, moneda destas, como ven al
turco agora: ese buen señor verá si le ha quedado alguna moneda
de plata, ó cuartos, y los repartirá entre ellas, que con poco
quedarán contentas.
—Sí traigo, dijo el galan.
Y sacó de la faldriquera tres reales de á ocho, que repartió entre
las tres jitanillas, con que quedaron mas alegres y mas satisfechas,
que suele quedar un autor de comedias cuando en competencia de
otro le suelen retular por las esquinas, victor, victor.
En resolucion concertaron, como se ha dicho, la venida de allí á
ocho dias, y que se habia de llamar cuando fuese jitano Andres
Caballero, porque tambien habia jitanos entre ellos deste apellido.
No tuvo atrevimiento Andres, que así le llamaremos de aquí
adelante, de abrazar á Preciosa, ántes enviándole con la vista el
alma, sin ella, si así decirse puede, las dejó, y se entró en Madrid, y
ellas contentísimas hicieron lo mismo. Preciosa, algo aficionada, mas
con benevolencia que con amor, de la gallarda disposicion de
Andres, ya deseaba informarse si era el que habia dicho: entró en
Madrid, y á pocas calles andadas encontró con el paje poeta de las
coplas y el escudo: y cuando él la vió, se llegó á ella diciendo:
—Vengas en buen hora, Preciosa; ¿leiste por ventura las coplas
que te di el otro dia?
Á lo que Preciosa respondió:
—Primero que le responda palabra, me ha de decir una verdad,
por vida de lo que mas quiere.
—Conjuro es ese, respondió el paje, que aunque el decirla me
costase la vida, no la negaré en ninguna manera.
—Pues la verdad que quiero que me diga, dijo Preciosa, es, si por
ventura es poeta.
—Á serlo, replicó el paje, forzosamente habia de ser por ventura;
pero has de saber, Preciosa, que ese nombre de poeta muy pocos le
merecen, y así yo no lo soy, sino un aficionado á la poesía: y para lo
que he menester, no voy á pedir ni buscar versos ajenos: los que te
di son mios, y estos que te doy agora tambien, mas no por esto soy
poeta, ni Dios lo quiera.
—¿Tan malo es ser poeta? replicó Preciosa.
—No es malo, dijo el paje; pero el ser poeta á solas no lo tengo
por muy bueno: hase de usar de la poesía, como de una joya
preciosísima, cuyo dueño no la trae cada dia, ni la muestra á todas
gentes, ni á cada paso, sino cuando convenga y sea razon que la
muestre: la poesía es una bellísima doncella, casta, honesta,
discreta, aguda, retirada, y que se contiene en los límites de la
discrecion mas alta: es amiga de la soledad, las fuentes la
entretienen, los prados la consuelan, los árboles la desenojan, las
flores la alegran; y finalmente, deleita y enseña á cuantos con ella
comunican.
 —Con todo eso, respondió Preciosa, he oido decir que es
pobrísima, y que tiene algo de mendiga.
—Antes es al reves, dijo el paje, porque no hay poeta que no sea
rico, pues todos viven contentos con su estado: filosofía que
alcanzan pocos. Pero ¿qué te ha movido, Preciosa, á hacer esta
pregunta?
—Hame movido, respondió Preciosa, porque como yo tengo á
todos, ó los mas poetas por pobres, causóme maravilla aquel escudo
de oro, que me distes entre vuestros versos envuelto: mas agora
que sé que no sois poeta, sino aficionado de la poesía, podria ser
que fuésedes rico, aunque lo dudo, á causa de que por aquella parte
que os toca de hacer coplas, se ha de desaguar cuanta hacienda
tuviéredes; que no hay poeta, segun dicen, que sepa conservar la
hacienda que tiene, ni granjear la que no tiene.
—Pues yo no soy desos, replicó el paje; versos hago, y no soy
rico, ni pobre: y sin sentirlo ni descontarlo, como hacen los jinoveses
sus convites, bien puedo dar un escudo, y dos á quien yo quisiere:
tomad, Preciosa perla, este segundo papel, y este escudo segundo
que va en él, sin que os pongais á pensar si soy poeta, ó no: solo
quiero que penseis y creais que quien os da esto, quisiera tener para
daros las riquezas de Midas.
Y en esto le dió un papel, y tentándole Preciosa halló que dentro
venia el escudo, y dijo:
—Este papel ha de vivir muchos años, porque trae dos almas
consigo; una la del escudo, y otra la de los versos, que siempre
vienen llenos de almas y de corazones; pero sepa el señor paje que
no quiero tantas almas conmigo, y si no saca la una, no haya miedo
que reciba la otra: por poeta le quiero, y no por dadivoso, y desta
manera tendremos amistad que dure; pues mas aina puede faltar un
escudo por fuerte que sea, que la hechura de un romance.
—Pues así es, replicó el paje, que quieres, Preciosa, que yo sea
pobre por fuerza, no deseches el alma que en ese papel te envío, y
vuélveme el escudo, que como le toques con la mano, le tendré por
reliquia miéntras la vida me durare.
Sacó Preciosa el escudo del papel, y quedóse con el papel, y no le
quiso leer en la calle. El paje se despidió y se fué contentísimo,
creyendo que ya Preciosa quedaba rendida, pues con tanta
afabilidad le habia hablado.
Y como ella llevaba puesta la mira en buscar la casa del padre de
Andres, sin querer detenerse á bailar en ninguna parte, en poco
espacio se puso en la calle do estaba, que ella muy bien sabia: y
habiendo andado hasta la mitad, alzó los ojos á unos balcones de
hierro dorados, que le habian dado por señas, y vió en ella á un
caballero de hasta edad de cincuenta años, con un hábito de cruz
colorada en los pechos, de venerable gravedad y presencia; el cual
apénas tambien hubo visto la Jitanilla, cuando dijo:
—Subid, niñas, que aquí os darán limosna.
Á esta voz acudieron al balcon otros tres caballeros, y entre ellos
vino el enamorado Andres, que cuando vió á Preciosa perdió la color,
y estuvo á punto de perder los sentidos: tanto fué el sobresalto que
recibió con su vista. Subieron las jitanillas todas, sino la grande que
se quedó abajo para informarse de los criados de las verdades de
Andres.
Al entrar las jitanillas en la sala, estaba diciendo el caballero
anciano á los demas:
—Esta debe de ser sin duda la Jitanilla hermosa, que dicen que
anda por Madrid.
—Ella es, replicó Andres, y sin duda es la mas hermosa criatura
que se ha visto.
—Así lo dicen, dijo Preciosa (que lo oyó todo en entrando); pero
en verdad que se deben de engañar en la mitad del justo precio:
bonita, bien creo que lo soy, pero tan hermosa como dicen, ni por
pienso.
—Por vida de D. Juanico mi hijo, dijo el anciano, que aun sois
mas hermosa de lo que dicen, linda jitana.
—Y ¿quién es D. Juanico su hijo? preguntó Preciosa.
—Ese galan que está á vuestro lado, respondió el caballero.
—En verdad que pensé, dijo Preciosa, que juraba vuesa merced
por algun niño de dos años: mirad qué D. Juanico, y qué brinco. Á
mi verdad que pudiera ya estar casado, y que segun tiene unas
rayas en la frente, no pasarán tres años sin que lo esté, y muy á su
gusto, si es que desde aquí allá no se le pierde, ó se le trueca.
 —Basta, dijo uno de los presentes: ¿qué sabe la Jitanilla de
rayas?
En esto las jitanillas que iban con Preciosa, todas tres se
arrimaron á un rincon de la sala, y cosiéndose las bocas unas con
otras, se juntaron por no ser oidas.
Dijo la Cristina:
—Muchachas, este es el caballero que nos dió esta mañana los
tres reales de á ocho.
—Así es la verdad, respondieron ellas; pero no se lo mentemos, ni
le digamos nada si él no nos lo mienta: ¿qué sabemos si quiere
encubrirse?
En tanto que esto entre las tres pasaba, respondió Preciosa á lo
de las rayas:
—Lo que veo con los ojos, con el dedo lo adevino: yo sé del señor
D. Juanico, sin rayas, que es algo enamoradizo, impetuoso y
acelerado, y gran prometedor de cosas que parecen imposibles; y
plegue á Dios que no sea mentirosito, que seria lo peor de todo: un
viaje ha de hacer agora muy léjos de aquí, y uno piensa el bayo, y
otro el que le ensilla: el hombre pone, y Dios dispone: quizá pensará
que va á Oñez, y dará en Gamboa.
Á esto respondió D. Juan:
—En verdad, jitanica, que has acertado en muchas cosas de mi
condicion; pero en lo de ser mentiroso vas muy fuera de la verdad,
porque me precio de decirla en todo acontecimiento: en lo del viaje
largo has acertado, pues sin duda siendo Dios servido, dentro de
cuatro ó cinco dias me partiré á Flándes, aunque tú me amenazas
que he de torcer el camino y no querria que en él me sucediese
algun desman que lo estorbase.
—Calle, señorito, respondió Preciosa, y encomiéndese á Dios, que
todo se hará bien; y sepa que yo no sé nada de lo que digo; y no es
maravilla, que como hablo mucho y á bulto, acierte en alguna cosa,
y yo querria acertar en persuadirte á que no te partieses, sino que
sosegases el pecho, y te estuvieses con tus padres para darles
buena vejez, porque no estoy bien con estas idas y venidas á
Flándes, principalmente los mozos de tan tierna edad como la tuya:
déjate crecer un poco para que puedas llevar los trabajos de la
guerra, cuanto mas que harta guerra tienes en tu casa, hartos
combates amorosos te sobresaltan el pecho: sosiega, sosiega,
alborotadito, y mira lo que haces primero que te cases, y dános una
limosnita por Dios, y por quien tú eres; que en verdad que creo que
eres bien nacido; y si á esto se junta el ser verdadero, yo cantaré la
gala al vencimiento de haber acertado en cuanto te he dicho.
—Otra vez te he dicho, niña, respondió el D. Juan, que habia de
ser Andres Caballero, que en todo aciertas, sino en el temor que
tienes, que no debo de ser muy verdadero, que en esto te engañas
sin alguna duda: la palabra que yo doy en el campo, la cumpliré en
la ciudad, y adonde quiera, sin serme pedida; pues no se puede
preciar de caballero quien toca en el vicio de mentiroso: mi padre te
dará limosna por Dios y por mí, que en verdad que esta mañana di
cuanto tenia á unas damas, que á ser tan lisonjeras como hermosas,
especialmente una dellas, no me arriendo la ganancia.
Oyendo esto Cristina, con el recato de la otra vez, dijo á las
demas jitanas:
—¡Ay, niñas! que me maten si no lo dice por los tres reales de á
ocho que nos dió esta mañana.
—No es así, respondió una de las dos, porque dijo que eran
damas, y nosotras no lo somos: y siendo él tan verdadero como
dice, no habia de mentir en esto.
—No es mentira de tanta consideracion, respondió Cristina, la que
se dice sin perjuicio de nadie y en provecho y crédito del que la dice;
pero con todo esto, veo no nos da nada, ni nos manda bailar.
Subió en esto la jitana vieja, y dijo:
—Nieta, acaba, que es tarde, y hay mucho que hacer y mas que
decir.
—Y ¿qué hay, abuela, preguntó Preciosa, hay hijo ó hija?
—Hijo, y muy lindo, respondió la vieja: ven, Preciosa, y oirás
verdaderas maravillas.
—Plega á Dios que no muera de sobreparto, dijo Preciosa.
—Todo se mirará muy bien, replicó la vieja, cuanto mas que hasta
aquí todo ha sido parto derecho, y el infante es como un oro.
—¿Ha parido alguna señora? preguntó el padre de Andres
Caballero:
 —Sí, señor, respondió la jitana; pero ha sido el parto tan secreto,
que le sabe sino Preciosa, y yo, y otra persona; y así no podemos
decir quién es.
—Ni aquí queremos saber, dijo uno de los presentes; pero
desdichada de aquella que en vuestras lenguas deposita su secreto y
en vuestra ayuda pone su honra.
—No todas somos malas, respondió Preciosa: quizá hay alguna
entre nosotras que se precia de secreta, y de verdadera, tanto
cuanto el hombre mas estirado que hay en esta sala: y vámonos,
abuela, que aquí nos tienen en poco; pues en verdad que no somos
ladronas, ni rogamos á nadie.
—No os enojeis, Preciosa, dijo el padre, que á lo ménos de vos
imagino que no se puede presumir cosa mala; que vuestro buen
rostro os acredita y sale por fiador de vuestras buenas obras: por
vida de Preciosita, que baileis un poco con vuestras compañeras,
que aquí tengo un doblon de oro de á dos caras, que ninguna es
como la vuestra, aunque son de dos reyes.
Apénas hubo oido esto la vieja, cuando dijo:
—Ea, niñas, haldas en cinta, y dad contento á estos señores.
Tomó las sonajas Preciosa, y dieron sus vueltas, hicieron y
deshicieron todos sus lazos con tanto donaire y desenvoltura, que
tras los piés se llevaban los ojos de cuantos las miraban,
especialmente los de Andres, que así se iban entre los piés de
Preciosa, como si allí tuvieran el centro de su gloria; pero turbósela
la suerte de manera que se la volvió en infierno; y fué el caso que
en la fuga del baile se le cayó á Preciosa el papel que le habia dado
el paje, y apénas hubo caido cuando le alzó el que no tenia buen
concepto de las jitanas, y abriéndole al punto dijo:
—Bueno, sonetico tenemos, cese el baile, y escúchenle, que
segun el primer verso, en verdad que no es nada necio.
Pesóle á Preciosa, por no saber lo que en él venia, y rogó que no
le leyesen y que se le volviesen, y todo el ahinco que en esto ponia,
eran espuelas que apremiaban el deseo de Andres para oirle.
Finalmente, el caballero le leyó en alta voz, y era este:
 Cuando Preciosa el panderete toca,
Y hiere el dulce son los aires vanos,
Perlas son que derrama con las manos,
Flores son que despide de la boca:
Suspensa el alma, y la cordura loca
Queda á los dulces actos sobrehumanos,
Que de limpios, de honestos y de sanos
Su fama al cielo levantado toca.
Colgadas del menor de sus cabellos
Mil almas lleva, y á sus plantas tiene
Amor rendidas una y otra flecha:
Ciega, y alumbra con sus soles bellos,
Su imperio amor por ellos le mantiene,
Y aun mas grandezas de su ser sospecha.

—Por Dios, dijo el que leyó el soneto, que tiene donaire el poeta
que le escribió.
—No es poeta, señor, sino un paje muy galan y muy hombre de
bien, dijo Preciosa.
Mirad lo que habeis dicho, Preciosa, y lo que vais á decir, que
esas no son alabanzas del paje, sino lanzas que traspasan el corazon
de Andres que las escucha: ¿quereislo ver, niña? pues volved los
ojos y veréisle desmayado encima de la silla con un trasudor de
muerte; no penseis, doncella, que os ama tan de burlas Andres, que
no le hiera y sobresalte el menor de vuestros descuidos: llegáos á él
enhorabuena, y decilde algunas palabras al oido que vayan derechas
al corazon, y le vuelvan de su desmayo: no, sino andáos á traer
sonetos cada dia en vuestra alabanza, y veréis cuál os le ponen.
Todo esto pasó así como se ha dicho, que Andres en oyendo el
soneto, mil celosas imaginaciones le sobresaltaron; no se desmayó,
pero perdió la color de manera que viéndole su padre, le dijo:
—¿Qué tienes, D. Juan, que parece que te vas á desmayar, segun
se te ha mudado el color?
 —Espérense, dijo á esta sazon Preciosa, déjenmele decir unas
ciertas palabras al oido, y verán cómo no se desmaya.
Y llegándose á él le dijo casi sin mover los labios:
—¡Gentil ánimo para jitano! ¿cómo podréis, Andres, sufrir el
tormento de toca, pues no podeis llevar el de un papel?
Y haciéndole media docena de cruces sobre el corazon, se apartó
dél; y entónces Andres respiró un poco, y dió á entender que las
palabras de Preciosa le habian aprovechado.
Finalmente, el doblon de dos caras se le dieron á Preciosa; y ella
dijo á sus compañeras que le trocaria y repartiria con ellas
hidalgamente. El padre de Andres le dijo que le dejase por escrito
las palabras que habia dicho á D. Juan, que las queria saber en todo
caso. Ella dijo que las diria de muy buena gana, y que entendiesen
que aunque parecian cosa de burla, tenian gracia especial para
preservar del mal el corazon y los vaguidos de cabeza, y que las
palabras eran:

Cabecita, cabecita,
Tente en tí, no te resbales,
Y apareja dos puntales
De la paciencia bendita.
Solicita
La bonita
Confiancita,
No te inclines
Á pensamientos ruïnes,
Verás cosas
Que toquen en milagrosas,
Dios delante
Y San Cristóbal gigante.

—Con la mitad destas palabras que le digan, y con seis cruces

que le hagan sobre el corazon á la persona que tuviere vaguidos de
cabeza, dijo Preciosa, quedará como una manzana.
Cuando la jitana vieja oyó el ensalmo y el embuste, quedó
pasmada, y mas lo quedó Andres que vió que todo era invencion de
su agudo ingenio. Quedáronse con el soneto, porque no quiso
pedirle Preciosa, por no dar otro tártago á Andres que ya sabia ella
sin ser enseñada lo que era dar sustos, martelos y sobresaltos
celosos á los rendidos amantes.
Despidiéronse las jitanas, y al irse dijo Preciosa á D. Juan:
—Mire, señor, cualquiera dia de esta semana es próspero para
partidas, y ninguno es aciago; apresure el irse lo mas presto que
pudiere, que le aguarda una vida ancha, libre y muy gustosa, si
quiere acomodarse á ella.
—No es tan libre la del soldado, á mi parecer, respondió D. Juan,
que no tenga mas de sujecion que de libertad; pero con todo esto
haré como viere.
—Mas veréis de lo que pensais, respondió Preciosa, y Dios os
lleve y traiga con bien como vuestra buena presencia merece.
Con estas últimas palabras quedó contento Andres, y las jitanas
se fueron contentísimas: trocaron el doblon, repartiéronle entre
todas igualmente, aunque la vieja guardiana llevaba siempre parte y
media de lo que se juntaba, así por la mayoridad, como por ser ella
el aguja por quien se guiaban en el maremagno de sus bailes,
donaires, y aun de sus embustes.
Llegóse en fin el dia que Andres Caballero se apareció una
mañana en el primer lugar de su aparecimiento sobre una mula de
alquiler, sin criado alguno; halló en él á Preciosa y á su abuela, de
las cuales conocido, le recibieron con mucho gusto. Él les dijo que le
guiasen al rancho ántes que entrase el dia, y con él se descubriesen
las señas que llevaba, si acaso le buscasen: ellas, que como
advertidas vinieron solas, dieron la vuelta, y de allí á poco rato
llegaron á sus barracas.
Entró Andres en una, que era la mayor del rancho, y luego
acudieron á verle diez ó doce jitanos, todos mozos y todos gallardos
y bien hechos, á quien ya la vieja habia dado cuenta del nuevo
compañero que les habia de venir, sin tener necesidad de
encomendarles el secreto, que como ya se ha dicho, ellos le guardan
con sagacidad y puntualidad nunca vista: echaron luego ojo á la
mula, y dijo uno dellos:
—Esta se podrá vender el juéves en Toledo.
 —Eso no, dijo Andres, porque no hay mula de alquiler que no sea
conocida de todos los mozos de mulas que trajinan por España.
—Par Dios, señor Andres, dijo uno de los jitanos, que aunque la
mula tuviera mas señales que las que han de preceder al dia
tremendo, aquí la transformarémos de manera que no la conociera
la madre que la parió, ni el dueño que la ha criado.
—Con todo eso, respondió Andres, por esta vez se ha de seguir y
tomar el parecer mio: á esta mula se le ha de dar muerte, y ha de
ser enterrada donde aun los huesos no parezcan.
—Pecado grande, dijo otro jitano: ¿á una inocente se ha de quitar
la vida? no diga tal el buen Andres, sino haga una cosa: mírela bien
agora, de manera que se le queden estampadas todas sus señales
en la memoria, y déjenmela llevar á mí, y si de aquí á dos horas la
conociera, que me lardeen como á negro fugitivo.
—En ninguna manera consentiré, dijo Andres, que la mula no
muera, aunque mas me aseguren su transformacion; yo temo ser
descubierto, si á ella no la cubre la tierra: y si se hace por el
provecho que de venderla puede seguirse, no vengo tan desnudo á
esta cofradía que no pueda pagar de entrada mas de lo que valen
cuatro mulas.
—Pues así lo quiere el señor Andres Caballero, dijo otro jitano,
muera la sin culpa, y Dios sabe si me pesa así por su mocedad, pues
aun no ha cerrado, cosa no usada entre mulas de alquiler, como
porque debe ser andariega, pues no tiene costras en las ijadas, ni
llagas de la espuela.
Dilatóse su muerte hasta la noche, y en lo que quedaba de aquel
dia se hicieron las ceremonias de la entrada de Andres á ser jitano,
que fueron: desembarazaron luego un rancho de los mejores del
aduar, y adornáronle de ramos y juncia, y sentándose Andres sobre
un medio alcornoque, pusiéronle en las manos un martillo y unas
tenazas, y al son de dos guitarras que dos jitanos tañian, le hicieron
dar dos cabriolas: luego le desnudaron un brazo, y con una cinta de
seda nueva y un garrote le dieron dos vueltas blandamente.
Á todo se halló presente Preciosa y otras muchas jitanas viejas y
mozas, que las unas con maravilla, otras con amor le miraban: tal
era la gallarda disposicion de Andres que hasta los jitanos le
quedaron aficionadísimos.
Hechas pues las referidas ceremonias, un jitano viejo tomó por la
mano á Preciosa, y puesto delante de Andres, dijo:
—Esta muchacha, que es la flor y la nata de toda la hermosura de
las jitanas que sabemos que viven en España, te la entregamos, ya
por esposa, ó ya por amiga, que en esto puedes hacer lo que fuere
mas de tu gusto, porque la libre y ancha vida nuestra no está sujeta
á melindres ni á muchas ceremonias: mírala bien, y mira si te
agrada, ó si ves en ella alguna cosa que te descontente, y si la ves,
escoge entre las doncellas que aquí están la que mas te contentare,
que la que escogieres te daremos; pero has de saber que una vez
escogida, no la has de dejar por otra, ni te has de empachar ni
entremeter ni con las casadas, ni con las doncellas: nosotros
guardamos inviolablemente la ley de la amistad: ninguno solicita la
prenda del otro; libres y ecsentos vivimos de la amarga pestilencia
de los celos: entre nosotros, aunque hay muchos incestos, no hay
ningun adulterio; y cuando le hay en la mujer propia, ó alguna
bellaquería en la amiga, no vamos á la justicia á pedir castigo;
nosotros somos los jueces y los verdugos de nuestras esposas ó
amigas: con la misma facilidad las matamos y las enterramos por las
montañas y desiertos, como si fueran animales nocivos: no hay
pariente que las vengue, ni padres que nos pidan su muerte: con
este temor y miedo ellas procuran ser castas, y nosotros, como ya
he dicho, vivimos seguros: pocas cosas tenemos que no sean
comunes á todos, excepto la mujer ó la amiga, que queremos que
cada una sea del que le cupo en suerte: entre nosotros así hace
divorcio la vejez como la muerte: el que quisiere puede dejar la
mujer vieja como él sea mozo, y escoger otra que corresponda al
gusto de sus años: con estas y con otras leyes y estatutos nos
conservamos y vivimos alegres: somos señores de los campos, de
los sembrados, de las selvas, de los montes, de las fuentes y de los
rios: los montes nos ofrecen leña de balde, los árboles frutas, las
viñas uvas, las huertas hortaliza, las fuentes agua, los rios peces, y
los vedados caza, sombras las peñas, aire fresco las quiebras, y
casas las cuevas: para nosotros las inclemencias del cielo son oreos,
refrigerio las nieves, baños la lluvia, músicas los truenos y hachas los
relámpagos: para nosotros son los duros terrenos colchones de
blandas plumas: el cuero curtido de nuestros cuerpos nos sirve de
arnes impenetrable que nos defiende: á nuestra lijereza no la
impiden grillos, ni la detienen barrancos, ni la contrastan paredes: á
nuestro ánimo no le tuercen cordeles, ni le menoscaban garruchas,
ni le ahogan tocas, ni le doman potros: del sí al no, no hacemos
diferencia cuando nos conviene; siempre nos preciamos mas de
mártires que de confesores: para nosotros se crian las bestias de
carga en los campos, y se cortan las faldriqueras en las ciudades: no
hay águila, ni ninguna otra ave de rapiña que mas presto se
abalance á la presa que se le ofrece, que nosotros nos abalanzamos
á las ocasiones que algun interes nos señalen: y finalmente,
tenemos muchas habilidades que felice fin nos prometen; porque en
la cárcel cantamos, en el potro callamos, de dia trabajamos, y de
noche hurtamos, y por mejor decir avisamos que nadie viva
descuidado de mirar donde pone su hacienda: no nos fatiga el temor
de perder la honra, ni nos desvela la ambicion del acrecentarla: ni
sustentamos bandos, ni madrugamos á dar memoriales, ni á
acompañar magnates, ni á solicitar favores: por dorados techos y
suntuosos palacios estimamos estas barracas y movibles ranchos:
por cuadros y países de Flándes los que nos da la naturaleza en esos
levantados riscos y nevadas peñas, tendidos prados y espesos
bosques que á cada paso á los ojos se nos muestran: somos
astrólogos rústicos, porque como casi siempre dormimos al cielo
descubierto, á todas horas sabemos las que son del dia y las que
son de la noche: vemos cómo arrincona y barre la aurora las
estrellas del cielo, y cómo ella sale con su compañera el alba,
alegrando el aire, enfriando el agua y humedeciendo la tierra, y
luego tras ella el sol, dorando cumbres (como dijo el otro poeta) y
rizando montes: ni tememos quedar helados por su ausencia cuando
nos hiere á soslayo con sus rayos, ni quedar abrasados cuando con
ellos perpendicularmente nos toca: un mismo rostro hacemos al sol
que al hielo, á la esterilidad que á la abundancia: en conclusion,
somos gente que vivimos por nuestra industria y pico, y sin
entremeternos con el antiguo refran: iglesia, ó mar, ó casa real,
tenemos lo que queremos, pues nos contentamos con lo que
tenemos: todo esto os he dicho, generoso mancebo, porque no
ignoreis la vida á que habeis venido, y el trato que habeis de
profesar, el cual os he pintado aquí en borron; que otras muchas é
infinitas cosas iréis descubriendo en él con el tiempo, no ménos
dignas de consideracion, que la que habeis oido.
Calló en diciendo esto el elocuente viejo jitano, y el novicio dijo,
que se holgaba mucho de haber sabido tan loables estatutos, y que
él pensaba hacer profesion en aquella órden tan puesta en razon y
en políticos fundamentos, y que solo le pesaba no haber venido mas
presto en conocimiento de tan alegre vida, y que desde aquel punto
renunciaba la profesion de caballero y la vanagloria de su ilustre
linaje, y lo ponia todo debajo del yugo, ó por mejor decir, debajo de
las leyes con que ellos vivian, pues con tan alta recompensa le
satisfacian el deseo de servirlos, entregándole á la divina Preciosa,
por quien él dejaria coronas é imperios, y solo los desearia para
servirla.
Á lo cual respondió Preciosa:
—Puesto que estos señores legisladores han hallado por sus leyes
que soy tuya, y que por tuya te me han entregado, yo he hallado
por la ley de mi voluntad, que es la mas fuerte de todas, que no
quiero serlo sino es con las condiciones que ántes que aquí vinieses
entre los dos concertamos: dos años has de vivir en nuestra
compañía primero que de la mia goces, porque tú no te arrepientas
por lijero, ni yo quede engañada por presurosa: condiciones rompen
leyes; las que te he puesto sabes, si las quisieres guardar, podrá ser
que sea tuya y tú seas mio; y donde no, aun no es muerta la mula,
tus vestidos están enteros, y de tu dinero no te falta un ardite: la
ausencia que has hecho no ha sido aun de un dia, que de lo que dél
falta te puedes servir y dar lugar que consideres lo que mas te
conviene: estos señores bien pueden entregarte mi cuerpo, pero no
mi alma, que es libre, y nació libre, y ha de ser libre en tanto que yo
quisiere: si te quedas, te estimaré en mucho; si te vuelves, no te
tendré en ménos, porque á mi parecer los ímpetus amorosos corren
á rienda suelta hasta que encuentran con la razon ó con el
desengaño: y no querria yo que fueses tú para conmigo como es el
cazador, que en alcanzando la liebre que sigue, la coge, y la deja por
correr tras otra que le huye: ojos hay engañados que á la primera
vista tan bien les parece el oropel como el oro, pero á poco rato bien
conocen la diferencia que hay de lo fino á lo falso: esta mi
hermosura, que tú dices que tengo, que la estimas sobre el sol y la
encareces sobre el oro, ¿qué sé yo si de cerca te parecerá sombra, y
tocada caerás en que es de alquimia? Dos años te doy de tiempo
para que tantees y ponderes lo que será bien que escojas, ó que
será justo que deseches: que la prenda que una vez comprada,
nadie se puede deshacer de ella sino con la muerte, bien es que
haya tiempo y mucho para miralla, y miralla, y ver en ella las faltas ó
las virtudes que tiene; que yo no me rijo por la bárbara é insolente
licencia que estos mis parientes se han tomado de dejar las mujeres,
ó castigarlas cuando se les antoja: y como yo no pienso hacer cosa
que llame al castigo, no quiero tomar compañía que por su gusto me
deseche.
—Tienes razon, ó Preciosa, dijo á este punto Andres; y así si
quieres que asegure tus temores, y menoscabe tus sospechas
jurándote que no saldré un punto de las órdenes que me pusieres,
mira qué juramento quieres que haga, ó qué otra seguridad puedo
darte; que á todo me hallarás dispuesto.
—Los juramentos y promesas que hace el cautivo porque le den
libertad, pocas veces se cumplen con ella, dijo Preciosa; y así son
segun pienso los del amante, que por conseguir su deseo prometerá
las alas de Mercurio, y los rayos de Júpiter, como me prometió á mí
un cierto poeta, y juraba por la laguna Estigia: no quiero
juramentos, señor Andres, ni quiero promesas; solo quiero remitirlo
todo á la esperiencia deste noviciado, y á mí se me quedará el cargo
de guardarme, cuando vos le tuviéredes de ofenderme.
—Sea así, respondió Andres: sola una cosa pido á estos señores y
compañeros mios, y es que no me fuercen á que hurte ninguna cosa
por tiempo de un mes siquiera, porque me parece que no he de
acertar á ser ladron, si ántes no preceden muchas liciones.
—Calla, hijo, dijo el jitano viejo, que aquí te industriaremos de
manera que salgas un águila en el oficio, y cuando le sepas has de
gustar dél, de modo que te comas las manos tras él: ¿ya es cosa de
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